Toxicological Research

Korean Society of Toxicology & Korea Environmental Mutagen Society (한국독성학회)
권호 표지
DOI QR코드

DOI QR Code

Dual oxidative stress and fatty acid profile impacts in Paracentrotus lividus exposed to lambda-cyhalothrin: biochemical and histopathological responses

  • Chaima Fouzai (Laboratory of Ecology, Biology and Physiology of aquatic organisms, Department of Biology, Faculty of Science, University of Tunis El Manar) ;
  • Wafa Trabelsi (Laboratory of Ecology, Biology and Physiology of aquatic organisms, Department of Biology, Faculty of Science, University of Tunis El Manar) ;
  • Safa Bejaoui (Laboratory of Ecology, Biology and Physiology of aquatic organisms, Department of Biology, Faculty of Science, University of Tunis El Manar) ;
  • Michel Marengo (Station de Recherche Sous-marines et Océanographiques (STARESO)) ;
  • Feriel Ghribi (Laboratory of Ecology, Biology and Physiology of aquatic organisms, Department of Biology, Faculty of Science, University of Tunis El Manar) ;
  • Imen Chetoui (Laboratory of Ecology, Biology and Physiology of aquatic organisms, Department of Biology, Faculty of Science, University of Tunis El Manar) ;
  • Sami Mili (Higher institute of fishing and aquaculture of Bizerte) ;
  • Nejla Soudani (Laboratory of Ecology, Biology and Physiology of aquatic organisms, Department of Biology, Faculty of Science, University of Tunis El Manar)
  • Received : 2022.10.19
  • Accepted : 2023.03.02
  • Published : 2023.07.15
⟨ Previous Next ⟩

Abstract

Lambda-cyhalothrin (λ-cyh) is a potential pyrethroid insecticide widely used in pest control. The presence of pyrethroids in the aquatic ecosystem may induce adverse effects on non-target organisms such as the sea urchin. This study was conducted to assess the toxic effects of λ-cyh on the fatty acid profiles, redox status, and histopathological aspects of Paracentrotus lividus gonads following exposure to three concentrations of λ-cyh (100, 250 and 500 ㎍/L) for 72 h. The results showed a significant decrease in saturated fatty acid (SFAs) with an increase in monounsaturated fatty acid (MUFAs) and polyunsaturated fatty acid (PUFAs) levels in λ-cyh treated sea urchins. The highest levels in PUFAs were recorded in the eicosapentaenoic acids (C20:5n-3), docosahexaenoic acids (C22:6n-3) and arachidonic acids (C20:4n-6) levels. The λ-cyh intoxication promoted oxidative stress with an increase in hydrogen peroxide (H2O2), malondialdehyde (MDA) and advanced oxidation protein products (AOPP) levels. Furthermore, the enzymatic activities and non-enzymatic antioxidants levels were enhanced in all exposed sea urchins, while the vitamin C levels were decreased in 100 and 500 ㎍/L treated groups. Our biochemical results have been confirmed by the histopathological observations. Collectively, our findings offered valuable insights into the importance of assessing fatty acids' profiles as a relevant tool in aquatic ecotoxicological studies.

Keywords

Acknowledgement

We are indebted to the editor and the anonymous reviewers for their acceptance to review this work.

References

  1. Boudouresque CH, Verlaque M (2007) Chap. 13 Ecology of Paracentrotus lividus. In Edible sea urchins: biology and ecology Edited by J.M. Lawrence. Elsevier B.V. 37:243-285. doi:https://doi.org/10.1016/s0167-9309(07)80077-9 
  2. Lozano J, Galera J, Lopez S et al (1995) Biological cycles and recruitment of Paracentrotus lividus (Echinodermata: Echinoidea) in two contrasting habitats. Mar Ecol Prog Ser 122:179-191. https://doi.org/10.3354/meps122179 
  3. Pesando D, Huiltorel P, Dolcinia V et al (2003) Biological targets of neurotoxic pesticides analysed by alteration of developmental events in the Mediterranean Sea urchin, Paracentrotus lividus. Mar Environ Res 55:39-57. https://doi.org/10.1016/s0141-1136(02)00215-5 
  4. Mol S, Baygar T, Varlik C, Tosun SY (2008) Seasonal variations in yield, fatty acids, amino acids and proximate compositions of sea urchin (Paracentrotus lividus) Roe. J Food Drug Anal 16:5. https://doi.org/10.38212/2224-6614.2363 
  5. Camacho C, Rocha AC, Barbosa VL et al (2018) Macro and trace elements in Paracentrotus lividus gonads from South West Atlantic areas. Environ Res 162:297-307. https://doi.org/10.1016/j.envres.2018.01.018 
  6. Zhou X, Zhou DY, Lu T et al (2018) Characterization of lipids in three species of sea urchin. Food Chem 241:97-103. https://doi.org/10.1016/j.foodchem.2017.08.076 
  7. Archana A, Babu KR (2016) Nutrient composition and antioxidant activity of gonads of sea urchin Stomopneustes variolaris. Food Chem 197:597-602. https://doi.org/10.1016/j.foodchem.2015.11.003 
  8. Siliani S, Melis R, Loi B et al (2016) Influence of seasonal and environmental patterns on the lipid content and fatty acid profiles in gonads of the edible sea urchin Paracentrotus lividus from Sardinia. Mar Environ Res 113:124-133. https://doi.org/10.1016/j.marenvres.2015.12.001 
  9. Martinez-Pita I, Garcia FJ, Pita ML (2010) The effect of seasonality on gonad fatty acids of the Sea Urchins Paracentrotus lividus and Arbacia lixula (Echinodermata: Echinoidea). J Shellfish Res 29:517-525. https://doi.org/10.2983/035.029.0231 
  10. Parrish CC (2013) Lipids in Marine Ecosystems. Int Sch Res Notices 2013:1-16. https://doi.org/10.5402/2013/604045 
  11. Berge JP, Barnathan G (2005) Fatty acids from lipids of Marine Organisms: Molecular Biodiversity, Roles as biomarkers, biologically active Compounds, and economical aspects. Adv Biochem Engin/Biotechnol 96:49-125. https://doi.org/10.1007/b135782 
  12. Zhu BW, Qin L, Zhou DY et al (2010) Extraction of lipid from sea urchin (Strongylocentrotus nudus) gonad by enzyme-assisted aqueous and supercritical carbon dioxide methods. Eur Food Res Technol 230:737-743. https://doi.org/10.1007/s00217-010-1216-8 
  13. Sanna R, Siliani S, Melis R et al (2017) The role of fatty acids and triglycerides in the gonads of Paracentrotus lividus from Sardinia: Growth, reproduction and cold acclimatization. Mar Environ Res 130:113-121. doi:https://doi.org/10.1016/j.marenvres.2017.07.003 
  14. Merzouk SA, Saker M, Reguig KB et al (2008) N-3 polyunsaturated fatty acids modulate In-Vitro T cell function in type I Diabetic patients. Lipids 43:485-497. https://doi.org/10.1007/s11745-008-3176-3 
  15. Goncalves AMM, Marques JC, Goncalves F (2017) Chap. 6 Fatty acids' profiles of aquatic organisms: revealing the impacts of environmental and anthropogenic stressors. In: Catala A (ed) Fatty acids. InTech, pp 89-117. https://doi.org/10.5772/intechopen.68544 
  16. Trabelsi W, Chetoui I, Fouzai C et al (2019) Redox status and fatty acid composition of Mactra corallina digestive gland following exposure to acrylamide. Environ Sci Pollut Res 26:22197-22208. https://doi.org/10.1007/s11356-019-05492-5 
  17. Maund SJ, Campbell PJ, Giddings JM et al (2011) Ecotoxicology of Synthetic Pyrethroids. Top Curr Chem 314:137-166. https://doi.org/10.1007/128_2011_260 
  18. He F (1994) Chap. 6 synthetic pyrethroids. Toxicology 91:43-49. https://doi.org/10.1016/0300-483X(94)90239-9 
  19. Maund SJ, Van Wijngaarden RPA, Roessink I et al (2008) Chap. 15 Aquatic fate and effects of lambda-cyhalothrin in model ecosystem experiments. In Gan (ed) Synthetic pyrethroids. Am Chem Soc Symp Ser. Washington, pp 335-354. https://doi.org/10.1021/bk-2008-0991.ch015 
  20. Zhou J, Kang HM, Lee YH, Jeong CB, Park JC, Lee JS (2019) Adverse effects of a synthetic pyrethroid insecticide cypermethrin on life parameters and antioxidant responses in the marine copepods Paracyclopina nana and Tigriopus japonicus. Chemosphere 217:383-392. https://doi.org/10.1016/j.chemosphere.2018.10.217 
  21. Farag MR, Alagawany M, Bilal RM et al (2021) An overview on the potential hazards of pyrethroid insecticides in Fish, with special emphasis on Cypermethrin Toxicity. Animals 11:1-17. https://doi.org/10.3390/ani11071880 
  22. Haya K (1989) Toxicity of pyrethroid insecticides to fish. Environ Toxicol Chem 8:381-391. https://doi.org/10.1002/etc.5620080504 
  23. Kumar A, Sharma B, Pandey RS (2008) Cypermethrin and λ-cyhalothrin induced alterations in nucleic acids and protein contentsin a freshwater fish, Channa punctatus. Fish Physiol Biochem 34:331-338. https://doi.org/10.1007/s10695-007-9192-z 
  24. United Nations Environment Programme, World Health Organization (WHO) & International Labour Organisation (1990) Cyhalothrin - Environmental health criteria 99. International Program on Chemical Safety, Geneva. https://wedocs.unep.org/20.500.11822/29411 
  25. Vieira CED, Dos Reis Martinez CB (2018) The pyrethroid λ-cyhalothrin induces biochemical, genotoxic, and physiological alterations in the teleost Prochilodus lineatus. Chemosphere 210:958-967. https://doi.org/10.1016/j.chemosphere.2018.07.115 
  26. Alvim TT, Martinez CB (2019) dos R Genotoxic and oxidative damage in the freshwater teleost Prochilodus lineatus exposed to the insecticides lambda-cyhalothrin and imidacloprid alone and in combination. Mutat Res/Genet Toxicol and Environ Mutagen. 842:85-93. https://doi.org/10.1016/j.mrgentox.2018.11.011 
  27. Bownik A, Kowalczyk M, Banczerowski J (2019) Lambda-cyhalothrin affects swimming activity and physiological responses of Daphnia magna. Chemosphere 216:805-811. https://doi.org/10.1016/j.chemosphere.2018.10.192 
  28. Fouzai C, Trabelsi W, Bejaoui S et al (2020) Cellular toxicity mechanisms of lambda-cyhalothrin in Venus verrucosa as revealed by fatty acid composition, redox status and histopathological changes. Ecol Indic 108:105690. https://doi.org/10.1016/j.ecolind.2019.105690 
  29. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275. https://doi.org/10.1016/S0021-9258(19)52451-6 
  30. Draper HH, Hadley M (1990) [43] Malondialdehyde determination as index of lipid peroxidation. Meth Enzymol 186:421-431. https://doi.org/10.1016/0076-6879(90)86135-I 
  31. Ou P, Wolff SP (1996) A discontinuous method for catalase determination at 'near physiological' concentrations of H2O2 and its application to the study of H2O2 fluxes within cells. J Biochemi Biophys Meth 31:59-67. https://doi.org/10.1016/0165-022X(95)00039-T 
  32. Kayali R, Cakatay U, Akcay T, Altug T (2006) Effect of alpha-lipoic acid supplementation on markers of protein oxidation in post-mitotic tissues of ageing rat. Cell Biochem Funct 24:79-85. https://doi.org/10.1002/cbf.1190 
  33. Ellman GL (1995) Tissue sulfhydryl groups. Arch Biochem and Biophysic 82:70-77. https://doi.org/10.1016/0003-9861(59)90090-6 
  34. Jacques-Silva MC, Nogueira CW, Broch LC et al (2001) Diphenyl diselenide and ascorbic acid changes deposition of selenium and ascorbic acid in liver and brain of mice: deposition of selenium and ascorbic acid in liver and brain of mice. Pharmacol Toxicol 88:119-125. https://doi.org/10.1034/j.1600-0773.2001.d01-92.x 
  35. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276-287. https://doi.org/10.1016/0003-2697(71)90370-8 
  36. Aebi H (1984) [13] catalase in vitro. Meth Enzymol 105:121-126. https://doi.org/10.1016/S0076-6879(84)05016-3 
  37. Flohe L, Gunzler WA (1984) [12] assays of glutathione peroxidase. Meth Enzymol 105:114-120. https://doi.org/10.1016/S0076-6879(84)05015-1 
  38. Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497-509. https://doi.org/10.1016/S0021-9258(18)64849-5 
  39. Cecchi G, Biasini S, Castano J (1985) Methanolyse rapide des huiles en solvants. Note de laboratoire. Rev Fr Corps Gras 32:163-164. http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=9170836 
  40. Martoja R, Martoja-Pierson M, Grasse PPP (1967) Initiation aux techniques de l'histologie animale. Masson et Cie, Paris, p 345 
  41. Sayeed I, Parvez S, Pandey S et al (2003) Oxidative stress biomarkers of exposure to deltamethrin in freshwater fish, Channa punctatus Bloch. Ecotoxicol Environ Saf 56:295-301. https://doi.org/10.1016/S0147-6513(03)00009-5 
  42. Erkmen B (2015) Spermiotoxicity and embryotoxicity of Permethrin in the Sea Urchin Paracentrotus lividus. Bull Environ Contam Toxicol 94:419-424. https://doi.org/10.1007/s00128-015-1482-z 
  43. Gharred T, Ezzine IK, Naija A et al (2015) Assessment of toxic interactions between deltamethrin and copper on the fertility and developmental events in the Mediterranean sea urchin, Paracentrotus lividus. Environ Monit Assess 187:193. https://doi.org/10.1007/s10661-015-4407-8 
  44. Tocher DR (2003) Metabolism and functions of lipids and fatty acids in Teleost Fish. Rev Fish Sci 11:107-184. https://doi.org/10.1080/713610925 
  45. Neves M, Castro BB, Vidal T et al (2015) Biochemical and populational responses of an aquatic bioindicator species, Daphnia longispina, to a commercial formulation of a herbicide (Primextra® Gold TZ) and its active ingredient (S-metolachlor). Ecol Indic 53:220-230. https://doi.org/10.1016/j.ecolind.2015.01.031 
  46. van der Merwe LF, Moore SE, Fulford AJ et al (2013) Long-chain PUFA supplementation in rural African infants: a randomized controlled trial of effects on gut integrity, growth, and cognitive development. Am J Clin Nutr 97:45-57. https://doi.org/10.3945/ajcn.112.042267 
  47. Kabeya N, Sanz-Jorquera A, Carboni S et al (2017) Biosynthesis of Polyunsaturated fatty acids in Sea Urchins: Molecular and Functional Characterisation of three fatty acyl desaturases from Paracentrotus lividus (Lamark 1816). PLoS One 12:e0169374. https://doi.org/10.1371/journal.pone.0169374 
  48. Hazel J (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29:167-227. https://doi.org/10.1016/0163-7827(90)90002-3 
  49. Arafa S, Chouaibi M, Sadok S, El Abed A (2012) The influence of season on the gonad index and biochemical composition of the Sea Urchin Paracentrotus lividus from the Golf of Tunis. Sci World J 2012:1-8. https://doi.org/10.1100/2012/815935 
  50. Yin X, Chen P, Chen H et al (2017) Physiological performance of the intertidal Manila clam (Ruditapes philippinarum) to long-term daily rhythms of air exposure. Sci Rep 7:41648. https://doi.org/10.1038/srep41648 
  51. Tallima H, El Ridi R (2018) Arachidonic acid: physiological roles and potential health benefits - A review. J Adv Res 11:33-41. https://doi.org/10.1016/j.jare.2017.11.004 
  52. Calder PC (2010) Omega-3 fatty acids and inflammatory processes. Nutrients 2:355-374. https://doi.org/10.3390/nu2030355 
  53. Zarrouk A, Ben Salem Y, Hafsa J et al (2018) 7β-hydroxycholesterol-induced cell death, oxidative stress, and fatty acid metabolism dysfunctions attenuated with sea urchin egg oil. Biochimie 153:210-219. https://doi.org/10.1016/j.biochi.2018.06.027 
  54. Gassner B, Wuthrich A, Scholtysik G et al (1997) The pyrethroids permethrin and cyhalothrin are potent inhibitors of the mitochondrial complex I. J Pharmacol Exp Ther 281:855-860 
  55. Regoli F, Giuliani ME (2014) Oxidative pathways of chemical toxicity and oxidative stress biomarkers in marine organisms. Mar Environ Res 93:106-117. https://doi.org/10.1016/j.marenvres.2013.07.006 
  56. Reeg S, Grune T (2015) Protein oxidation in aging: does it play a role in aging progression? Antioxid Redox Signal 23:239-255. https://doi.org/10.1089/ars.2014.6062 
  57. El-Demerdash FM (2007) Lambda-cyhalothrin-induced changes in oxidative stress biomarkers in rabbit erythrocytes and alleviation effect of some antioxidants. Toxicol in Vitro 21:392-397. https://doi.org/10.1016/j.tiv.2006.09.019 
  58. Slaninova A, Smutna M, Modra H et al (2009) A review: oxidative stress in fish induced by pesticides. Neuro Endocrinol Lett 30(Suppl 1):2-12 
  59. Ullah S, Li Z, Zain M, Ullah KS, Shah F (2019) Multiple biomarkers based appraisal of deltamethrin induced toxicity in silver carp (Hypophthalmichthys molitrix). Chemosphere 214:519-533. https://doi.org/10.1016/j.chemosphere.2018.09.145 
  60. Pisoschi AM, Pop A (2015) The role of antioxidants in the chemistry of oxidative stress: a review. Euro J Med Chem 97:55-74. https://doi.org/10.1016/j.ejmech.2015.04.040 
  61. Das D, Moniruzzaman M, Sarbajna A et al (2017) Effect of heavy metals on tissue-specific antioxidant response in indian major carps. Environ Sci Pollut Res 24:18010-18024. https://doi.org/10.1007/s11356-017-9415-5 
  62. Dringen R, Gutterer JM, Hirrlinger J (2000) Glutathione metabolism in brain: metabolic interaction between astrocytes and neurons in the defense against reactive oxygen species. Euro J Biochem 267:4912-4916. https://doi.org/10.1046/j.1432-1327.2000.01597.x 
  63. KhazriA, SellamiB, Dellali M et al(2015)Acute toxicity of cypermethrin on the freshwater mussel Unio gibbus. Ecotoxicol Environ Saf 115:62-66. https://doi.org/10.1016/j.ecoenv.2015.01.028 
  64. Au DWT (2004) The application of histo-cytopathological biomarkers in marine pollution monitoring: a review. Mar Pollut Bull 48:817-834. https://doi.org/10.1016/j.marpolbul.2004.02.032 
  65. Ortiz-Zarragoitia M, Cajaraville MP (2006) Biomarkers of exposure and Reproduction-Related Effects in Mussels exposed to endocrine disruptors. Arch Environ Contam Toxicol 50:361-369. https://doi.org/10.1007/s00244-005-1082-8 
  66. Schafer S, Kohler A (2009) Gonadal lesions of female sea urchin (Psammechinus miliaris) after exposure to the polycyclic aromatic hydrocarbon phenanthrene. Mar Environ Res 68:128-136. https://doi.org/10.1016/j.marenvres.2009.05.001 
  67. Walker CW (1982) Nutrition of gametes. In: Jangoux M, Lawrence JM (eds) Echinoderm nutrition. Balkema, Rotterdam, Netherlands, pp 449-468 
  68. Unuma T (2002) Gonadal growth and its relationship to aquaculture in sea urchins. In: Yokota Y, Matranga V, Smolenicka Z (eds) The sea urchin: from basic biology to aquaculture. Swets & Zeitlinger, Lisse, Netherlands, pp 115-127 
  69. Unuma T, Yamamoto T, Akiyama T, Shiraishi M, Ohta H (2003) Quantitative changes in yolk protein and other components in the ovary and testis of the sea urchin Pseudocentrotus depressus. J Exp Biol 206:365-372. https://doi.org/10.1242/jeb.00102 
  70. Unuma T, Sawaguchi S, Yamano K et al (2011) Accumulation of the Major yolk protein and zinc in the Agametogenic Sea Urchin gonad. Biol Bull 221:227-237. https://doi.org/10.1086/BBLv221n2p227 
  71. Marsh AG, Powell ML, Watts SA (2013) Biochemical and energy requirements of gonad development. In: Lawrence JM (ed) Sea urchins: biology and ecology, 3rd edn. Elsevier, Amsterdam, Netherlands, pp 45-57