Abstract
Many biochemical, physiological and histological criteria have been used as indicators of exposures and effects of the contaminants. These changes can indicate the response of an organism to a specific environmental stressor. In the present paper, the effect of the acute and chronic exposure to cadmium as well as recovery from two cadmium concentrations (10 and 30 μgCd/g dry food) on gypsy moth (Lymantria dispar) midgut esterases was investigated. The influence of cadmium on trait plasticity was also examined. Esterases showed great sensitivity to low metal concentrations during acute and chronic treatments. Their activities during short-term exposure and after recovery significantly depended on cadmium concentrations. The esterases had greater index of plasticity during chronic treatments with 10 and 30 μgCd/dry food. Five esterase isoforms between 64 and 250 kDa were detected. Isoforms of esterases exposed to any of the two cadmium effects differed among several egg-masses. Isozymes were distinguished in one egg-mass during different cadmium treatments. We conclude that these enzymes could be considered potential and sensitive non-selective biomarkers for the presence of cadmium in food.
Similar content being viewed by others
References
Allderdice PW, Garner HAR, Galutira D, Lockridge O, LaDu BN, McAlpines J (1991) The cloned butyrylcholinesterase (BCHE) gene maps to a single chromosome site. Genomics 11:452–454
Augustyniak M, Migula P (2000) Body burden with metals and detoxifying abilities of the grasshopper—Chorthippus brunneus (Thunberg) from industrially polluted areas. In: Markert B, Frieze K (eds) Trace Metals in the Environment. Elsevier, Amsterdam, pp 423–454
Bell RA, Owens, CD, Shapiro M, Tardif JR (1981) Mass rearing and virus production: development of mass-rearing technology. In: Doane CC, McManus ML (eds) The gypsy moth: research toward integrated pest management, vol. 614. USDA For: Serv Tech Bull no. 1584
Blackstock J (1984) Biochemical metabolic regulatory responses of marine invertebrates to natural environmental change and marine pollution. Oceanogr Mar Biol Annu Rev 22:263–313
Bogaerts P, Senaud J, Bohatier J (1998) Bioassay technique using nonspecific esterase activities of Tetrahymena pyriformis for screening and assessing cytotoxicity of xenobiotics. Environ Toxicol Chem 17:1600–1605
Bradford M (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Braeckman B, Raes H, Van Hoye D (1997) Heavy-metal toxicity in an insect cell line. Effects of cadmium chloride, mercuric chloride and methylmercuric chloride on cell viability and proliferation in Aedes albopictus cells. Cell Biol Toxicol 13:389–397
Braeckman B, Brys K, Rzeznik U, Raes H (1999) Cadmium pathology in an insect cell line: ultrastructural and biochemical effects. Tissue Cell 3:45–53
Burbank S, Snell TW (1994) Rapid toxicity assessment using esterase biomarkers in Brachionus calyciflorus (Rotifera). Environ Toxicol Water Qual 9:171–178
Callaghan A, Parker PJAN, Holloway GJ (1998) 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 12:436–441
Carfagna MA, Ponsler GD, Muhoberac BB (1996) Inhibition of ATPase activity in rat synaptic plasma membranes by simultaneous exposure to metals. Chem Biol Interact 100:53–65
Chatonnet A, Lockridge O (1989) Comparision of butyrylcho-linesterase and acetylcholinesterase. Biochem J 260:625–634
Cheplick GP (1995) Genotypic variation and plasticity of clonal growth in relation to nutritient availability in Amphibromus scabrivalvis. J Ecol 83:459–468
Clark AG (1989) The comparative enzymology of the glutathione S-transferases from non-vertebrate organisms. Comp Biochem Physiol B 92:419–446
Çokuğraş AN (2003) Butyrylcholinesterase: Structure and Physiological Importance. Turk J Biochem 28:54–61
Costa JRMA, Mela M, de Assis HCS, Pelletier E, Randi MAF, de Oliveira Ribeiro CA (2007) Enzymatic inhibition and morphological changes in Hoplias malabaricus from dietary exposure to lead (II) or methylmercury. Ecotoxicol Environ Saf 67:82–88
Dauterman WC (1985) Insect metabolism: extramicrosomal. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology biochemistry and pharmacology. Pergamon, Oxford, pp 713–730
Dave KR, Syal AR, Katyare SS (2000) Tissue cholinesterases. A comparative study of their kinetic properties. Z Naturforsch 55c:100–108
De Coen WM, Janssen CR (1997) The use of biomarkers in Daphnia magna testing: 2. Digestive activity in Daphnia magna exposed to sublethal concentrations of cadmium, chromium and mercury. Chemosphere 25:1053–1076
De Coen WM, Vangheluwe ML, Janssen CR (1998) The use of biomarkers in Daphnia magna toxicity testing. III. Rapid toxicity testing of pure chemicals and sediment pore waters using ingestion and digestive activity. Chemosphere 37:2677–2694
Diamantino TC, Almeida E, Soares AMVM, Guilhermino L (2003) Characterization of Cholinesterases from Daphnia magna Straus and Their Inhibition by Zinc. Bull Environ Contam Toxicol 71:219–225
Doane CC, McManus ML (1981) The gypsy moth: research toward integrated pest management. USDA Forest Service Technical Bulletin 1584:1757
Duan Y, Guttman SI, Oris JT, Bailer AJ (2001) Differential survivorship among allozyme genotypes of Hyalella azteca exposed to cadmium, zinc or low pH. Aquat Toxicol 54:15–28
Dubovskiy IM, Martemyanov BB, Vorontsova YL, Rantala MJ, Gryzanova EV, Glupov VV (2008) Effect of the bacterial infection on the antioxidant activity and lipid peroxidation in the midgut of larvae Galleria mellonella L. (Lepidoptera, Pyralidae). Comp Biochem Physiol 148C:1–5
Fournier D, Bride JM, Poire M, Berge JB, Plapp FW (1992) Insect glutathione S-transferases. Biochemical characteristics of the major forms from houseflies susceptible and resistant to insecticides. J Biol Chem 267:1840–1845
Frasco MF, Colletier JP, Weik M, Carvalho F, Guilhermino L, Stojan J, Fournier D (2007) Mechanisms of cholinesterase inhibition by inorganic mercury. FEBS J 274:1849–1861
Grafton-Cardwell E, Ouyang Y, Salse J (1998) Insecticide resistance and esterase enzyme variation in the California Red Scale (Homoptera: Diaspidae). J Econ Entomol 91:812–819
Guilhermino L, Barros P, Silva MC, Soares AMVM (1998) Should the use of inhibition of cholinesterase as a specific biomarker for organophosphate and carbamate pesticides be questioned? Biomarkers 3(2):157–163
Guttman SI (1994) Population genetic structure and ecotoxicology. Environ Health Perspect 102(Suppl 12):97–100
Habig C, DiGiulio RT (1991) Biochemical characteristics of cholinesterases in aquatic organisms. In: Mineau P (ed) Cholinesterase inhibiting insecticides: Their impact on wildlife and environment. Elsevier, Amsterdam, pp 19–33
Hodgson E (2004) A textbook of modern toxicology. John Wiley & Sons Inc, New Jersey
Jacobson KB, Turner JE (1980) The interaction of cadmium and certain other metal ions with proteins and nucleic acids. Toxicology 16:1–37
Jones BR, Bancroft HR (1986) Distribution and probable physiological role of esterases in reproductive, digestive and fat-body tissue of adult cotton boll weevil, Anthonomus grandis. Biochem Genet 24:499–508
Kapin MA, Ahmad S (1980) Esterases in larval tissue of gypsy moth Lymantria dispar (L): optimum assay conditions, quantification and characterization. Insect Biochem 10:331–337
Knežević J (2004) Analysis of pollutant contents in the air and precipitation – EMEP Station Kamenički Vis. In: Kadović R and Knežević M (eds) Forest Condition Monitoring in the Republic of Serbia, Annual report ICP Forests 2003, Level I. Ministry of Science and Environmental Protection of Serbia, FineGRAF
Kort CAD, Granger NA (1981) Regulation of the juvenile hormone titer. Ann Rev Entomol 26:1–28
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Levins R (1968) Evolution in changing environments. Princeton Univ. Press, New Jersey
Lockridge O, La Du BN (1978) Comparison of atypical and usual human serum cholinesterase. J Biol Chem 253:361–366
Loxdale HD (1983) Electrophoretic study of enzymes from cereal aphid populations. I. Electrophoretic techniques and staining system for characterising isozymes from six species of cereal aphids (Homoptera: Aphididae). Bull Entomol Res 73:645–657
Mane SD, Tompkins L, Richmond RC (1983) Male esterase—6 catalyzes the synthesis of a sex pheromone in Drosophila melanogaster females. Science 222:419–421
Marczyk G, Migula P, Trzcionka E (1993) Physiological response of spiders to environmental pollution in the Silesian region (Southern Poland). Sci Total Environ (Suppl 2):1315–1322
McCarthy JF, Shugart LR (1990) Biomarkers of environmental contamination. Lewis Publishers, Boca Raton
O’Dell TM, Bell RA, Mastro VC, Tanner JA, Kennedy JF (1984) Production of the gypsy moth, Lymantria dispar, for research and biological control. In: King EG, Leppla NC (eds) Advanced and challenges in insect rearing. USDA-ARS, New Orleans, pp 156–166
Prabhakaran SK, Kamble ST (1995) Purification and characterization of an esterase isozyme from insecticide resistant and susceptible strains of German cockroach. Blattella germanica (L.). Insect Biochem Mol Biol 25:519–524
Satyavathi C, Prabhakara Rao Y (2000) Inhibition of Na+, K+-ATPase in Penaeus indicus postlarvae by lead. Comp Biochem Physiol 127C:11–22
Scheiner SM, Goodnight CJ (1984) The comparison of phenotypic plasticity and genetic variation in populations of the grass Danthonia spicata. Evolution 38:845–855
Scheiner SM, Caplan RL, Lyman RF (1991) The genetics of phenotypic plasticity, III. Genetics correlations and fluctuating asymmetries. J Evol Biol 4:51–68
Serebrov VV, Gerber ON, Malyarchuk AA, Martemyanov VV, Alekseev AA, Glupov VV (2006) Effect of entomopathogenic fungi on detoxification enzyme activity in greater wax moth Galleria mellonella L. (Lepidoptera, Pyralidae) and role of detoxification enzymes in development of insect resistance to entomopathogenic fungi. Biol Bull 33:581–586
Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Rad Biol Med 18:321–336
Stone D, Jepson P, Laskowski R (2002) Trends in detoxification enzymes and heavy metals accumulation in ground beetles (Coleoptera, Carabidae) inhabiting a gradient of pollution. Comp Biochem Physiol C 132:105–112
Tavares MG, Ceron CR, Azeredo-Oliveira MTV (1998) Tissue-specific expression of esterases in Triatoma infestans (Triatominae, Heteroptera). Genet Mol Biol 21:461–464
Terra WR, Ferreira C, Jordao BP, Dillon RJ (1996) Digestive enzymes. In: Lehane MJ, Billingsley PF (eds) Biology of insect midgut. Chapman & Hall, London, pp 153–186
Turunen S, Chippendale GM (1977) Ventricular esterases: comparison of their distribution within the larval midgut of four species of Lepidoptera. Ann Entomol Soc Am 70:146–149
Van Straalen NM, Donker MH (1994) Heavy metal adaptation in terrestrial arthropods—physiological and genetic aspects. In: Sommeijer MJ, Van der Blom J (eds) Proceedings of the section experimental and applied entomology of the Netherlands Entomological Society (N. E. V.). Netherlands Entomological Society, Amsterdam, pp 3–17
Vlahović M, Ilijin L, Lazarević J (2001) Acute effect of cadmium on larval growth of Lymantria dispar L. Ekologija 36:132–137
Vlahović M, Lazarević J, Perić-Mataruga V, Ilijin L, Mrdaković M (2009) Plastic response of larval mass and alkaline phosphatase to cadmium in the gypsy moth larvae. Ecotoxicol Environ Saf 72:1148–1155
WHO (1992a) Environmental Health Criteria 134: Cadmium. World Health Organization, Geneva
WHO (1992b) Environmental Health Criteria 135: Cadmium—environmental aspects. World Health Organization, Geneva
Wilczek G, Migula P (1996) Metal body burdens and detoxifying enzymes in spiders from industrially polluted areas. Fresenius J Anal Chem 354:643–667
Wilczek G, Majkus Z, Migula P, Bednarska K, Swierczek E (1997) Heavy metals and detoxifying enzymes in spiders from coal and metallurgic dumps near Ostrava (Czech Republic). In: Proceedings of the 16th European colloidal arachnology, pp 317–328
Wilczek G, Babczynska A, Migula P, Wencelis B (2003) Activity of esterases as biomarkers of metal exposure in spiders from metal pollution gradient. Pol J Environ Stud 12:765–771
Zhu KY, Brindley WA (1990) Properties of esterases from Lygus hesperus Knight (Hemiptera: Miridae) and the roles of the esterases in insecticide eresistance. J Econ Entomol 83:725–732
Zvereva E, Serebrov V, Glupov V, Dubovskiy I (2003) Activity of heavy metal resistance of non-specific esterases in leaf beetle Chrysomela lapponica from polluted and unpolluted habitats. Comp Biochem Physiol C 135:383–391
Acknowledgment
This study was supported by the Serbian Ministry of Education and Science (grant No.173027).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Vlahović, M., Perić Mataruga, V., Ilijin, L. et al. Changes in activity of non-specific esterases in cadmium treated Lymantria dispar larvae. Ecotoxicology 21, 370–378 (2012). https://doi.org/10.1007/s10646-011-0798-7
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-011-0798-7