Benzo[a]pyrene-induced changes in carboxylesterase, acetylcholinesterase and heat shock protein 70 of Lymantria dispar (Lepidoptera: Lymantriidae) from unpolluted and polluted forests
Keywords:
Lymantria dispar L., brain tissue, benzo[a]pyrene, esterase, Hsp70, polycyclic aromatic hydrocarbons (PAHs), environmental pollutionAbstract
Paper description:
- Anthropogenic activities are responsible for increased concentrations of the pollutant benzo[a]pyrene in the environment.
- Identifying molecular indicators of stress induced by benzo[a]pyrene in a widespread insect species, Lymantria dispar has great importance in pollution biomonitoring. Two populations of Lymantria dispar larvae from different habitats were fed on benzo[a]pyrene. Carboxylesterases, acetylcholinesterase and heat shock protein 70 from larva brain tissue served as molecular parameters of sensitivity to benzo[a]pyrene presence.
- Carboxylesterases and Hsp70 were sensitive to low benzo[a]pyrene concentrations and population pre-exposure history, with a dependent response recorded.
- Different pollution biomarkers are suitable for different Lymantria dispar populations.
Abstract: Plant vegetation accumulates polycyclic aromatic hydrocarbons (PAHs) among which benzo[a]pyrene (B[a]P) is recognized as being very toxic, including cancerogenic. Lymantria dispar L. larvae are sensitive to changes in the environment, providing potential signs of pollutant presence. We examined the chronic effects of two concentrations of B[a]P on the activity of carboxylesterase (CaE), acetylcholinesterase (AChE) and heat shock protein 70 (Hsp70) levels in the brain tissue of two populations of L. dispar larvae, originating from unpolluted and polluted habitats. We found that the relative growth rate was significantly lower in both populations and that only larvae from polluted forests were sensitive to low B[a]P concentrations, exhibiting a significant increase in brain tissue CaE activity and Hsp70 concentration. AChE activity showed no changes in response to B[a]P exposure in either population. Examined biochemical parameters indicate that their sensitivity to chronic treatment with B[a]P was highly dependent on the pre-exposure history of L. dispar larvae, suggesting that they could be promising biomarkers of B[a]P and PAH pollution in forest ecosystems.
https://doi.org/10.2298/ABS190620056G
Received: June 20, 2019; Revised: July 30, 2019; Accepted: August 28, 2019; Published online: September 6, 2019
How to cite this article: Grčić A, Ilijin L, Mrdaković M, Vlahović M, Filipović A, Đurašević S, Perić-Mataruga V. Benzo[a]pyrene-induced changes in carboxylesterase, acetylcholinesterase and heat shock protein 70 of Lymantria dispar (Lepidoptera: Lymantriidae) from unpolluted and polluted forests. Arch Biol Sci. 2019;71(4):735-45.
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References
Douben PET. PAHs: An Ecotoxicological Perspective. West Sussex, UK: John Wiley and Sons; 2003. 392 p.
Fernandez P, Grimalt JO, Vilanova RM. Atmospheric gas/particle partitioning of polycyclic aromatic hydrocarbons in high mountain regions of Europe. Environ Sci Technol. 2002;36:1163-8.
Wilcke W. Global patterns of polycyclic aromatic hydrocarbons (PAHs) in soil. Geoderma. 2007;141:157-66.
US Environmental Protection Agency. Polycyclic organic matter (POM) [Internet]. Washington, D.C: US Environmental Protection Agency; 1992 Apr [updated 2000 Jan; cited 2013 Dec 16]. Available from: https://www.epa.gov/sites/production/files/2016-09/documents/polycyclic-organic-matter.pdf
EEA: Air Quality in Europe - 2012 Report, EEA Report No 4/2012 [Internet]. Copenaghen: European Environment Agency; 2012. [cited 2013 Dec 16]. Available from: https://www.eea.europa.eu/publications/air-quality-in-europe-2012
Collins CD, Finnegan E. Modeling the plant uptake of organic chemicals, including the soil-air-plant pathway. Environ Sci Technol. 2010;44:998-1003.
Desalme D, Binet P, Chiapusio G. Challenges in tracing the fate and effects of atmospheric polycyclic aromatic hydrocarbon deposition in vascular plants. Environ Sci Technol. 2013;47:3967-81.
De Nicola F, Concha Graña E, López Mahía P, Muniategui Lorenzo S, Prada Rodríguez D, Retuerto R, Carballeira A, Aboa JR, Fernández JÁ. Evergreen or deciduous trees for capturing PAHs from ambient air? A case study. Environ Pollut. 2017;221:276-84.
Howsam M, Jones KC, Ineson P. PAHs associated with the leaves of three deciduous tree species, I - concentrations and profiles. Environ Pollut. 2000;18:413-24.
Liebhold AM, Gottschalk KW, Muzika RM, Montgomery ME, Young R, O’Day K, Kelley B. Suitability of North American Tree Species to the Gypsy Moth: a Summary of Field and Laboratory Tests. Morgantown, WV, USA: Northeastern Forest Experiment Station, USDA Forest Service; 1995. 34 p. General Technical Report NE-211.
McCarty LS, Power M, Munkittrick KR. Bioindicators versus biomarkers in ecological risk assessment. Hum Ecol Risk Assess. 2002;8(1):159-64.
Matić D, Vlahović M, Kolarević S, Perić-Mataruga V, Ilijin L, Mrdaković M, Vuković Gačić B. Genotoxic effects of cadmium and influence on fitness components of Lymantria dispar caterpillars. Environ Pollut. 2016;218:1270-7.
Gavrilović A, Ilijin L, Mrdaković M, Vlahović M, Mrkonja A, Matić D, Perić-Mataruga V. Effects of benzo[a]pyrene dietary intake to antioxidative enzymes of Lymantria dispar (Lepidoptera:Lymantriidae) larvae from unpolluted and polluted forests. Chemosphere. 2017;179:10-9.
Van Brummelen TC, Stuijfzand SC. Effects of benzo[a]pyrene on survival, growth and energy reserves in the terrestrial isopods Oniscus asellus and Porcellio scaber. Sci Total Environ. 1993;134:921-30.
Mrdaković M, Ilijin L, Vlahović M, Todorović D, Gavrilović A, Mrkonja A, Perić-Mataruga, V. Effects offluoranthene on thefitness-related traits and antioxidative defense in Lymantria dispar L. Environ Sci Pollut Res. 2015;22:10367-74.
Perić-Mataruga V, Petković B, Ilijin L, Mrdaković M, Dronjak Čučaković S, Todorović D, Vlahović M. Cadmium and high temperature effects on brain and behaviour of Lymantria dispar. L. caterpillars originating from polluted and less-polluted forests. Chemosphere. 2017;185:628-36
Satoh T, Hosokawa M. Structure, function and regulation of carboxylesterases. Chem Biol Interact. 2006;162(3):195-211.
Kapin MA, Ahmad S. Esterases in larval tissues of gypsy moth, Lymantria dispar (L.): Optimum assay conditions, quantification and characterization. Insect Biochem. 1980;10:331-7.
Jones BR, Bancroft HR. Distribution and probable physiological role of esterases in reproductive, digestive and fat-body tissue of adult cotton boll weevil, Anthonomus grandis. Biochem Genet. 1986;24:499-508.
Hemingway J, Hawkes N, McCarroll L; Ranson H. The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Mol Biol. 2004;34(7):653-65.
Richardson BJ, Mak E, De Luca-Abott SB, Martin M, McLellan K, Lam PKS. Antioxidant responses to polyclic aromatic hydrocarbons and organochloride pesticides in green-lipped mussels (Perna viridis): Do mussels “integrate” biomarker response. Mar PollutBull. 2008;57:503-14.
Galloway TS, Handy R. Immunotoxicity of organophosphorous pesticides. Ecotoxicology. 2003;12:345-63.
Senthil Nathan S, Choi MY, Seo HY, Paik CH, Kalaivani K, Kim JD. Effect of azadirachtin on acetylcholinesterase (AChE) activity and histology of the brown planthopper Nilaparvata lugens (Stål). Ecotox Environ Safe. 2008;70:244-50.
Jett DA, Navoa RV, Lyons MAJr. Additive inhibitory actions of chlorpyrifos and polycyclic aromatic hydrocarbons on acetylcholinesterase activity in vitro. Toxicol Lett. 1999;105:223-9.
Kang JJ, Fang HW. Polycyclic aromatic hydrocarbons inhibit the activity of acetylcholinesterase purified from electric eel. Biochem Biophys Res Commun. 1997;238:367-9.
Lewis S, Handy RD, Cordi B, Billinghurst Z, Depledge MH. Stress proteins (HSP’s): methods of detection and their use as an environmental biomarker. Ecotoxicology. 1999;8:351-69.
Köhler HR, Knödler C, Zanger M. Divergent kinetics of hsp70 induction in Oniscus asellus (isopoda) in response to four environmentally relevant organic chemicals (B[a]P, PCB52, g-HCH, PCP): suitability and limits of a biomarker. Arch Environ Contam Toxicol. 1999;36:179-85.
Morales M, Planello R, Martínez-Paz P, Herrero O, Cortes E, Martínez Guitarte, JL, Morcillo, G. Characterization of Hsp70 gene in Chironomus riparius: expression in response to endocrine disrupting pollutants as a marker of ecotoxicological stress. Comp Biochem Physiol C. 2011;153:150-8.
Živković M, Jovašević-Stojanović M, Cvetković A, Lazović I, Tasić V, Stevanović Ž, Gržetić I. PAHs levels in gas and particle-bound phase in schools at different locations in Serbia. Chem Ind Chem Eng. Q. 2015;21:159-67.
Alagić S, Stankov-Jovanović V, Mitić V, Cvetković J, Petrović G, Stojanović G. Bioaccumulation of HMW PAHs in the roots of wild blackberry from the Bor region (Serbia): phytoremediation and biomonitoring aspects. Sci Total Environ. 2016;562:561-70.
O'Dell TM, Butt CA, Bridgeforth AW. Lymantria dispar. In: Singh P, Moore RF, editors. Handbook of Insect Rearing. New York: Elsevier; 1985. p. 355-67.
Bradford MM. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of proteindye binding. Anal Biochem. 1976:72:248-54.
Main AR, Miles KE, Braid PE. The Determination of Human-Serum-Cholinesterase Activity with o-Nitrophenyl Butyrate. Biochem J. 1961;78:769-76.
Ellman GL, Courtney KO, Anders V, Featherstone RM. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol. 1961;7:88-95.
Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680-5.
Gottlieb LD. Genetic confirmation of the origin of Clarkia lingulata. Evolution. 1974;28:244-50.
Karnovsky MJ, Roots L. A "Direct-coloring" thiocholine method for cholinesterase. J Histochem Cytochem. 1964;12:219-21.
Prud'homme SM, Chaumot A, Cassar E. David JP, Reynaud S. Impact of micropollutants on the life-history traits of the mosquito Aedes aegypti: On the relevance of transgenerational studies. Environ Pollut. 2017;220(Part A):242-54.
Van Straalen NM, Hoffmann, A. Review of experimental evidence for physiological costs of tolerance to toxicants. In: Kammenga J, Laskowski R, editors. Demography in Ecotoxicology. Chichester, UK: John Wiley & Sons Ltd.; 2000. p. 147-61.
Ilijin L, Mrdaković M, Todorović D, Vlahović M, Gavrilović A, Mrkonja A, Perić-Mataruga V. Life history traits and the activity of antioxidative enzymes in Lymantria dispar L. (Lepidoptera, Lymantriidae) larvae exposed to benzo[a] pyrene. Environ Toxicol Chem. 2015;34(11):2618-24.
Bergman A, Heindel JJ, Jobling S, Kidd KA, Zoeller RT, editors. State of the science of endocrine disrupting chemicals - 2012 : an assessment of the state of the science of endocrine disruptors prepared by a group of experts for the United Nations Environment Programme (UNEP) and WHO. Geneva, Switzerland: United National Environment Programme; 2013. 296 p.
Thomas P. Teleost model for studying the effects of chemicals on female reproductive endocrine function. J Exp Zool Suppl. 1990;4:126-8.
Panini M, Manicardi GC, Moores GD, Mazzoni E. An overview of the main pathways of metabolic resistance in insects. Invert Surviv J. 2016;13:326-35.
Callaghan A, Parker PJAN, Holloway GJ. The use of variance in enzyme activity as an indicator of long-term exposure test to toxicant-stressed environments in Culex pipens mosquitoes. Funct Ecol. 1998;12:436-44.
Migula P, Glowacka E, Nuorteva SL, Nuorteva P, Tulisalo E. Time related effects of intoxication with cadmium and mercury in the red wood ants (Formica aquilonia). Ecotoxicology. 1997;6:307-20.
Vlahović M, Perić-Mataruga V, Ilijin L, Mrdaković M, Mirčić D, Todorović D, Lazarević J. Changes in activity of non-specific esterases in cadmium treated Lymantria dispar larvae. Ecotoxicology. 2012;21:370-8.
Miller KP, Ramos KS. Impact of cellular metabolism on the biological effects of benzo[a]pyrene and related hydrocarbons. Drug Metab Rev. 2001;33:1-35.
Lionetto MG, Caricato R, Calisi A, Schettino T. Acetylcholinesterase inhibition as a relevant biomarker in environmental biomonitoring: New insights and perspectives. In: Visser JE, editor. Ecotoxicology around the Globe. New York: Nova Science Publishers Inc.; 2011. p. 87-115.
Perić-Mataruga V. Vlahović M, Mrdaković M, Matić D, Gavrilović A, Mrkonja A, Ilijin L. Ghrelin effects on midgut tissue and antioxidative defense and gluthatione S-transferase activity in Lymantria dispar (Lepidoptera). Turkish J Biol. 2015;39:618-23.
Ilijin L, Mrdaković M, Vlahović M, Matić D, Gavrilović A, Mrkonja A, Perić-Mataruga V. Acetylcholinesterase and heat shock protein 70 response in larval brain tissue of Lymantria dispar L. (Lepidoptera, Limantriidae) upon chronic exposure to benzo[a]pyrene. Environ Sci Pollut Res. 2017;24(25):20818-23.
Mrdaković M, Ilijin L, Vlahović M, Matić D, Gavrilović A, Mrkonja A, Perić-Mataruga V. Acetylcholinesterase (AChE) and heat shock proteins (Hsp70) of gypsy moth (Lymantria dispar L.) larvae in response to long-term fluoranthene exposure. Chemosphere. 2016;159:565-9.
Van Brummelen TC, Van Straalen NM. Uptake and elimination of benzo[a]pyrene in the terrestrial isopod Porcellio scaber. Arch Environ Contam Toxicol. 1996;31(2):277-85.
Escartin E, Porte C. The use of cholinesterase and carboxylesterase activities from Mytilus galloprovincialis in pollution monitoring. Environ Toxicol Chem. 1997;16;2090-5.
Wogram J, Sturm A, Segner H, Liess M. Effects of parathion on acetylcholinesterase, butyrylcholinesterase, and carboxylesterase in three-spined stickleback ( Gasterosteus aculeatus) following short-term exposure. Environ Toxicol Chem. 2001;20:1528-31.
Lee SM, Lee SB, Park CH, Choi J. Expression of heat shock protein and hemoglobin genes in Chironomus tentans (Diptera, Chironomidae) larvae exposed to various environmental pollutants: a potential biomarker of freshwater monitoring. Chemosphere. 2006;65:1074-81.
Cruz-Rodriguez LA, Chu FLE. Heat-shock protein (HSP70) response in the eastern oyster, Crassostrea irginica, exposed to PAHs sorbed to suspended artificial clay particles and to suspended field contaminated sediments. Aquatic Toxicol. 2002;60:157-68.
Dinan L, Bourne P, Whiting P, Dhaidalla TS, Hutchinson TH. Screening of environmental contaminants for ecdysteroid agonist and antagonist activity using the Drosophila melanogaster BII cell in vitro assay. Environ Toxicol Chem. 2001;20:2038-46.
Gupta SC, Sharma A, Mishra M, Mishra RK, Chowdhuri DK. Heat shock proteins in toxicology: how close and how far? Life Sci. 2010;86:377-84.
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