Immunotoxicity and lysosomal damage on Pinctada imbricata (Röding) exposed to used automobile crankcase oils
DOI:
https://doi.org/10.25268/bimc.invemar.2024.53.1.1208Keywords:
Hemocyte; lysosomal destabilization; oil; immunology; stressAbstract
The effect of exposure to water-soluble fractions of used automobile crankcase oils (WSF-AUCO) on haematology parameters, immune system, stability of lysosomal membranes of hemocytes and lipid peroxidation in the digestive gland of the pearl oyster Pinctada imbricata was evaluated in this study. The oysters were exposed to 0, 1, 10 and 20 % v/v of WSF-AUCO during different periods: 3, 5 and 7 d, in static aquaria under controlled conditions (oxygenation 6 mg/L; 25 ± 1 °C; pH 8.0 and 36 ‰). During the early period (3d) of exposure, an increase in the total count of hemocytes (TCH) was observed to 10 % of WSF-AUCO. In oyster exposed to 20 % during 7 d significant decreases in immuno-hematological parameters associated with high lysosomal destabilization of hemocytes
and malondialdehyde (MDA) concentration was observed. The oysters showed compensatory cellular responses to the WSF-AUCO low concentrations, but these decreased during acute exposure. Immuno-modulator effects were induced by complex mixtures of compounds of WSF-AUCO. The molecular and immune-cellular responses estimated in P. imbricada offer appropriate information on the change in
the normal physiology of organisms that inhabit impacted environments by complex mixtures of xenobiotics.
References
Aliko, V., G. Hajdaraj, A. Caci and C. Faggio. 2015. Copper induced lysosomal membrane destabilisation in haemolymph cells of mediterranean green
crab (Carcinus aestuarii, Nardo, 1847) from the Narta Lagoon (Albania). Braz. Arch. Biol. Technol. 58(5):750–756. https://doi.org/10.1590/s1516-
Allam, B. and D. Raftos. 2015. Immune responses to infectious diseases in bivalves. J. Invert. Pathol., 131: 121–136. https://doi.org/10.1016/j.jip.2015.05.005
Auguste, M., Balbi, T., Ciacci, C., Canonico, B., Papa, S., Borello, A., Vezzulli, L., Canesi, L. 2020. Shift in immune parameters after repeated exposure to
nanoplastics in the marine bivalve Mytilus. Front Immunol. 15: 11:426. https://doi.org/10.3389/fimmu.2020.00426
Auguste, M., T. Balbi, C. Ciacci, B. Canonico, S. Papa, A. Borello, L. Vezzulli, L. Canesi, L. 2020. Shift in immune parameters after repeated exposure to
nanoplastics in the marine bivalve Mytilus. Front Immunol. 15: 11:426. https://doi.org/10.3389/fimmu.2020.00426
Bachère, E., R.D. Rosa, P.M. Schmitt, A. Poirier and N. Merou. 2015. The new insights into the oyster antimicrobial defense: cellular, molecular and genetic
view. Fish and Shellfish Immunology, 2015, 46 (1), pp.50-64. https://doi.org/10.1016/j.fsi.2015.02.040
Balbi, T., M. Auguste, C. Ciacci and L. Canesi. 2021. Immunological Responses of Marine Bivalves to Contaminant Exposure: Contribution of the -Omics
Approach. Front Immunol. 12: 618726. https://doi.org/10.3389/fimmu.2021.618726
Basria, S.M.N., R.I. Mydin and S. Okekpa. 2019. Reactive oxygen species, cellular redox homeostasis and cancer. homeostasis–an integrated vision. In:
Lasacosvitsch F, S. Dos Anjos Garnes (Eds) BiotechOpen, London. https://doi.org/10.5772/intechopen.76096
Burgos-Aceves, M. A. and C. Faggio. 2017. An approach to the study of the immunity functions of bivalve haemocytes: Physiology and molecular aspects.
Fish & Shellfish Immunology, 67, 513–517. https://doi.org/10.1016/j.fsi.2017.06.042
Cvengros, J., T. Liptaj and N. Pónayová. 2017. Study of polyaromatic hydrocarbons in current used motor oils, Int. J. Petrochem. Sci. Eng., 2(7) 219-226.
https://doi.org/10.15406/ipcse.2017.02.00060
Freitas, J.S., T.S. Boscolo-Pereira, C.N. Pereira-Boscolo, M. Navarro-García, C.A. de Oliveira-Rivero and E.A. De Almeida. 2020. Oxidative stress,
biotransformation enzymes and histopathological alterations in Nile tilapia (Orechromis niloticus) exposed to new and used automotive lubricant oil.
Comp. Physiol., 234: 1-11. https://doi.org/10.1016/j.cbpc.2020.108770
Goven, A. and J. Kennedy. 1996. Environmental pollution and toxicity in invertebrates: An earthworm model for immunotoxicology. Adv. Comp. Environ.
Physiol., 24: 170-211. https://doi.org/10.1007/978-3-642-79847-4_7
He, L., T. He, S. Farrar, L. Ji, T. Liu and X. Ma. 2017. Antioxidants maintain cellular redox homeostasis by elimination of reactive oxygen species. Cell
Physiol. Biochem., 44: 532-553. https://doi.org/10.1159/000485089
Hwang, H.M., B. Stanton, T. Mcbride and M. Anderson. 2014. Polycyclic aromatic hydrocarbon body residues and lysosomal membrane destabilization
in mussels exposed to the Dubai Star bunker fuel oil (intermediate fuel oil 380) spill in San Francisco Bay. Environ. Toxicol. Chem., 33: 1117–1121.
https://doi.org/10.1002/etc.2518
Jiang Y, Tang X, Sun T, Wang and Y. BDE-47 Exposure Changed the Immune Function of Haemocytes in Mytilus edulis: An Explanation Based on ROSMediated
Pathway. Aquat Toxicol (2017) 182:58–66. https://doi.org/10.1016/j.aquatox.2016.11.010
Liao, Y., C. Cai, C. Yang, Z. Zheng, Q. Wang, X. Du and Y. Deng. 2020. Effect of protein sources in formulated diets on the growth, immune response, and
intestinal microflora of pearl oyster Pinctada fucata martensii. Aquac. Rep., 16: 100253. https://doi.org/10.1016/j.aqrep.2019.100253
Lodeiros, C.J., L. Freites, A. Márquez, M.E. Glem, M. Guevara and P.E. Saucedo. 2016. Comparative growth and survival of spat of the Caribbean pearl oyster,
Pinctada imbricata cultivated indoor with microalgae diets and outdoor with natural diet. Aquacul. Nutr., 23(3): 511–522. https://doi.org/10.1111/anu.12419
López-Landavery, E.A., G. Amador-Cano, M.A. Tripp-Valdez, N. Ramírez-Álvarez, F. Cicala, R.J.E. Gómez-Reyes, F. Díaz, A.D. Re-Araujo and C.E.
Galindo-Sánchez. 2022. Hydrocarbon exposure effect on energetic metabolism and immune response in Crassostrea virginica. Marine Pollution Bulletin.
:113738. https://doi.org/10.1016/j.marpolbul.2022.113738.
Lowe, D., M. Moore and B. Evans. 1992. Contaminant impact of interactions of molecular probes with lysosomes in living hepatocytes from dab Limanda
limanda. Mar. Ecol. Prog. Ser., 91 (1): 135-140. https://doi.org/10.3354/meps091135
Lowry, O., N. Rosebroungh, A. Farr and R. Randall. 1951. Protein measurement with the folin reagent. J. Biol. Chem., 193: 265-275.
Mansour, C., F.B. Taheur and R. Omrani. 2020. Immune biomarker and hydrocarbon concentrations in carpet shell clams (Ruditapes decussatus) collected
from a Mediterranean coastal lagoon. Euro-Mediterr J. Environ. Integr., 5: 11. https://doi.org/10.1007/s41207-020-0147-4
Martínez-Gómez, C., J. Benedicto, J.A. Campillo and M. Moore. 2008. Application and evaluation of the neutral red retention (NRR) assay for lysosomal
stability in mussel populations along the Iberian Mediterranean coast. J. Environ. Monit., 10(4): 490. https://doi.org/10.1039/b800441m
Matozzo, V., M. Giacomazzo, L. Finos, M.G. Marin, L. Bargelloni and M. Milan. 2013. Can ecological history influence immunomarker responses and
antioxidant enzyme activities in bivalves that have been experimentally exposed to contaminants? A new subject for discussion in “eco-immunology”
studies. Fish Shell. Immunol., 35(1): 126–135. https://doi.org/10.1016/j.fsi.2013.04.013
Méthé, D., L.A. Comeau, H. Stryhn, J.F. Burka, T. Landry and J. Davidson. 2017. Haemolymph fluid osmolality influences the neutral-red retention assay
in the eastern oyster Crassostrea virginica, J. Molluscan Stud. 83: 229–234. https://doi.org/10.1093/mollus/eyw050
Nusetti, O., L. Marcano, E. Zapata, M. Escalpés, S. Nusetti y C. Lodeiros. 2004. Respuestas inmunológicas y de enzimas antioxidantes en la ostra perla Pinctada
imbricata (Mollusca: Pteridae) expuesta a niveles subletales de fuel oil Nº6. Interciencia, 29(6): 324-328. http://ve.scielo.org/scielo.php?script=sci_
arttextypid=S0378-18442004000600008ylng=esynrm=iso
Ohkawa, H., N. Ohishi and K. Yagi. 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction, Rev. Anal. Biochem. 95: 351–358.
https:// doi. org/10.1016/0003-2697(79)90738
Olonisakin, A., A. Adebayo and M.O. Aremu. 2005. Metal concentrations of fresh, used and treated crankcase oil. Biosci. Biotech. Res. Asia; 3: 187-191.
Available from: http://www.biotech-asia.org/?p=4361
Parisi, M.G., J. Pirrera, C.M. La Corte, D. Dara, M. Parrinello and Cammarata. 2021. Effects of organic mercury on Mytilus galloprovincialis hemocyte
function and morphology. J. Comp. Physiol. B; 191: 143–158. https://doi.org/10.1007/s00360-020-01306-0
Renault, T. 2015. Immunotoxicological effects of environmental contaminants on marine bivalves. Fish Shellfish Immunol., 46(1): 88–93. https://doi.
org/10.1016/j.fsi.2015.04.011
Romero-Fereira, P., D. Arrieche, V. Acosta, L. Pérez and C. Lodeiros. 2017. Gametogenic cycle of the oyster, Pinctada imbricata, in suspended culture in
the Gulf of Cariaco, Venezuela. Lat. Am. J. Aquat. Res.;45(1): 139-148. https://doi.org/10.3856/vol45-issue1-fulltext-13
Sun, S., W. Shi, Y. Tang, Y. Han, X. Du, W. Zhou, Y. Hu, C. Zhou and G. Liu. 2020. Immunotoxicity of petroleum hydrocarbons and microplastics alone
or in combination to a bivalve species: Synergic impacts and potential toxication mechanisms. Sci. Total Environm., 728: https://doi.org/10.1016/j.
scitotenv.2020.138852
Strober, W. 2015. Trypan blue exclusion test of cell viability. Curr. Protoc. Im. 2 111, https://doi.org/10.1002/0471142735.ima03bs111
Sokal, R. and F. Rohlf. 2012. Biometry. 4th Ed. W.H. Freeman. New York.
Trivedi, P.C., J.J. Bartlett and T. Pulinilkunnil. 2020. Lysosomal biology and function: Modern view of cellular debris bin. Cells, 9(5): 1131. https://
doi. org/10.3390/cells9051131
Vásquez, G., R. Crescini, W. Villalba, J. Mogollón y L. Troccoli. 2015. Aspectos biológicos básicos de Pinctada imbricata (Bivalvia: Pteriidae) en la laguna
de La Restinga, isla de Margarita, Venezuela. Rev, Cienc. Mar. Cost.,7: 117-132. https://doi.org/10.15359/revmar.7.8
Villegas, L., C. Lodeiros, K. Malavé, J. Revilla y M. Lemus. 2015. Efecto subletal del cadmio en la ostra perla del Caribe Pinctada imbricata (Pteroida:
Pteriidae) Röding, 1798. Saber; 27 (1): 39-45
Week, J., V. Sharp and T. Williams. 1997. Contaminant-induced lisosomal membrane damage in blood cells of green mussel Perna viridis (Mytilidae): a
field transplant study. Technical Report WC/97/64. DFID-TDR Proyect R6191. Land-derived contaminant influx to Jakarta Bay, Indonesia; 2: 1-30.
Wei J., B Liu, S Fan, B Zhang, J Su and D. Yu. 2017. Serum immune response of pearl oyster Pinctada fucata to xenografts and allografts. Fish Shellfish
Immunol., 62: 303-310. https://doi.org/10.1016/j.fsi.2017.01.039
Xie, J., C. Zhao, Q. Han, H. Zhou, Q. Li and X. Diao. 2017. Effects of pyrene exposure on immune response and oxidative stress in the pearl oyster, Pinctada
martensii. Fish Shellfish Immunol., 63: 237–244. https://doi.org/10.1016/j.fsi.2017.02.032
Zha, S., J. Rong, X. Guan, Y. Tang, Y. Han and G. Liu. 2019. Immunotoxicity of four nanoparticles to a marine bivalve species, Tegillarca granosa. J. Hazard
Mater 377:237–48. https://doi.org/10.1016/j.jhazmat.2019.05.071
Zannella, C., F. Mosca, F. Mariani, G. Franci, V. Folliero, M. Galdiero, P.G. Tiscar and M. Galdiero. 2017. Microbial diseases of bivalve mollusks: infections,
immunology and antimicrobial defense. Mar. Drugs; 15(6):182. https://doi.org/10.3390/md15060182
Zapata-Vívenes, E., L. Marcano y V. Acosta 2018. Respuestas inmunológicas, estabilidad lisosomal y frecuencia de micronúcleos en Eurythoe
complanata (Polychaeta:Amphinomidae) expuestos a una fracción acuosa de lubricantes usados de motores de automóviles. Rev. Intern. Contam.
Amb., 34 (2): 297-305. https://doi.org/10.20937/RICA.2018.34.02.10
Zapata-Vívenes, E., O. Nusetti, L. Marcano, G. Sánchez and H. Guderley. 2020. Antioxidant defenses of flame scallop Ctenoides scaber (Born, 1778) exposed
to the water-soluble fraction of used vehicle crankcase oils. Toxicol. Rep., 7:1597–1606. https://doi.org/10.1016/j.toxrep.2020.11.009
Zapata Vívenes, E., G. Sánchez, O. Nusetti and L. Marcano. 2022. Modulation of innate immune responses in the flame scallop Ctenoides scaber (Born,
caused by exposure to used automobile crankcase oils, Fish & Shellfish Immunology, 130: 342- 349. https://doi.org/10.1016/j.fsi.2022.09.020
Zhao, C., L. Xiaoxu, L. Shibin and Y. Chang. 2011. Assessments of lysosomal membrane responses to stresses with neutral red retention assay and its potential
application in the improvement of bivalve aquaculture. Afr, J. Biotechnol., 10 (64): 13968- 3973. https://doi.org/10.5897/AJB10.2283
Zheng, F., F. Marques Gonçalves, Y. Abiko, H. Li, Y. Kumagai and M. Aschner. 2020. Redox toxicology of environmental chemicals causing oxidative stress.
Redox Biol., 34: https://doi.org/10.1016/j.redox.2020.101475
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 Edgar Alexander Zapata Vivenes, Gabreial Sanchez, Leida Marcano
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
