Dose-dependent alteration in hepatic and cerebral glucose metabolism following exposure to polystyrene microplastic in Wistar rats

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Published: Mar 30, 2024
DOI: https://doi.org/10.55184/ijpas.v76i01.213
Keywords:
Polystyrene microplastics; energy metabolism; glycolysis; gluconeogenesis; TCA cycle; transaminase function

Main Article Content

Sudipta Pal
Nutritional Biochemistry and Toxicology Laboratory, Department of Human Physiology, Tripura University.
https://orcid.org/0000-0002-0969-3662
Susmita Chakraborty
Nutritional Biochemistry and Toxicology Laboratory, Department of Human Physiology, Tripura University.
Sumana Mondal
Nutritional Biochemistry and Toxicology Laboratory, Department of Human Physiology, Tripura University.

Abstract

Background: Recently, microplastics (MPs) with dimensions less than 5 mm have gained more attention due to their adverse impact on the environment and living creatures. Polystyrene (PS) particle is a key element of primary microplastics, which are causing numerous health issues such as interruption of energy metabolism, oxidative stress, neurotoxicity, immunotoxicity, digestive gland disorders, reproductive disruption, and genotoxicity in marine living organisms. Method: Alteration in carbohydrate metabolism was evaluated in male Wistar rats (six weeks of age) after four weeks of oral exposure to polystyrene microplastic (PS-MP) at three different doses (0.5mg/L, 5mg/L and 50 mg/L via drinking water). Results: Polystyrene exposure caused a significant decrease in blood glucose, liver glycogen, and pyruvic acid content in liver and cerebral tissue. Free amino nitrogen content significantly altered in the liver and cerebrum in a dose-specific manner. The LDH activity was found to be decreased in the liver, whereas it increased in the cerebral cortex of rats in a dose-responsive fashion. Enzymes like glucose 6-phosphatase, GOT, GPT, and succinate dehydrogenase activities demonstrated differential effects on the liver and cerebrum of rats in terms of energy metabolism. Conclusion: It is suggested that sub-acute polystyrene exposure significantly perturbs glucose metabolism by inducing hypoglycemia associated with decreased glycolysis and increased TCA cycle enzyme function in rat liver in a dose-dependent manner. Gluconeogenesis is also affected differentially by metabolic adjustment in the studied organs.

Article Details

How to Cite
Pal, S., Chakraborty, S. ., & Mondal, S. (2024). Dose-dependent alteration in hepatic and cerebral glucose metabolism following exposure to polystyrene microplastic in Wistar rats. INDIAN JOURNAL OF PHYSIOLOGY AND ALLIED SCIENCES, 76(01), 32–39. https://doi.org/10.55184/ijpas.v76i01.213
Issue
Vol. 76 No. 01 (2024): INDIAN JOURNAL OF PHYSIOLOGY AND ALLIED SCIENCES
Section
Research Article

References

Zhang Q, Zhao Y, Du F, Cai H, Wang G, Shi H. Microplastic fallout in different indoor environments. Environ Sci Tech. 2020;54(11):6530-9. DOI: 10.1021/acs.est.0c00087.

Campanale C, Massarelli C, Savino I, Locaputo V, Uricchio VF. A detailed review study on potential effects of microplastics and additives of concern on human health. Int J Environ Res Public Health. 2020;17(4):1212. DOI:10.3390/ijerph17041212.

Wang J, Li Y, Lu L, et al. Polystyrene microplastics cause tissue damages, sex-specific reproductive disruption and transgenerational effects in marine medaka (Oryzias melastigma). Environ Pollution. 2019;254:113024. DOI: 10.1016/j.envpol.2019.113024.

Hwang J, Choi D, Han S, Jung SY, Choi J, Hong J. Potential toxicity of polystyrene microplastic particles. Sci Rep. 2020;10(1):1-2. DOI:10.1038/s41598-020-64464-9.

Ding N, Jiang L, Wang X, et al. Polyethylene microplastic exposure and concurrent effect with Aeromonas hydrophila infection on zebrafish. Enviorn Sci Pollut Res. 2022;29(42):63964-72. DOI:10.1007/s11356-022-20308-9.

Turner A. Foamed polystyrene in the marine environment: sources, additives, transport, behavior, and impacts. Environ Sci Technol. 2020;54(17):10411-20. DOI: 10.1021/acs.est.0c03221.

Huang W, Wang X, Chen D, et al. Toxicity mechanisms of polystyrene microplastics in marine mussels revealed by high- coverage quantitative metabolomics using chemical isotope labeling liquid chromatography mass spectrometry. J Hazard Mater. 2021;417:126003. DOI: 10.1016/j.jhazmat.2021.126003.

Sussarellu R, Suquet M, Thomas Y, Lambert C, Fabioux C, Pernet ME, Le Goïc N, Quillien V, Mingant C, Epelboin Y, Corporeau C. Oyster reproduction is affected by exposure to polystyrene microplastics. PNAS. 2016;113(9):2430-5. DOI:10.1073/pnas.1519019113.

Lee HS, Amarakoon D, Wei CI, Choi KY, Smolensky D, Lee SH. Adverse effect of polystyrene microplastics (PS-MPs) on tube formation and viability of human umbilical vein endothelial cells. Food Chem Toxicol. 2021;154:112356. DOI:10.1016/j.fct.2021.112356.

Qiao R, Sheng C, Lu Y, Zhang Y, Ren H, Lemos B. Microplastics induce intestinal inflammation, oxidative stress, and disorders of metabolome and microbiome in zebrafish. Sci Total Environ. 2019;662:246-53. DOI:10.1016/j.scitotenv.2019.01.245.

Xie X, Deng T, Duan J, Xie J, Yuan J, Chen M. Exposure to polystyrene microplastics causes reproductive toxicity through oxidative stress and activation of the p38 MAPK signaling pathway. Ecotoxicol Environmental Safety. 2020;190:110133. DOI: 10.1016/j.ecoenv.2019.110133.

Zhao Y, Bao Z, Wan Z, Fu Z, Jin Y. Polystyrene microplastic exposure disturbs hepatic glycolipid metabolism at the physiological, biochemical, and transcriptomic levels in adult zebrafish. Sci Total Environ. 2020;710:136279. DOI: 10.1016/j.scitotenv.2019.136279.

Barboza LG, Vieira LR, Branco V, et al. Microplastics cause neurotoxicity, oxidative damage and energy-related changes and interact with the bioaccumulation of mercury in the European seabass, Dicentrarchus labrax (Linnaeus, 1758). Aqua Toxicol. 2018;195:49-57. DOI:10.1016/j.aquatox.2017.12.008.

Luo T, Zhang Y, Wang C, et al. Maternal exposure to different sizes of polystyrene microplastics during gestation causes metabolic disorders in their offspring. Environmental Poll. 2019;255:113122. DOI:10.1016/j.envpol.2019.113122.

Cheng W, Li X, Zhou Y, et al. Polystyrene microplastics induce hepatotoxicity and disrupt lipid metabolism in the liver organoids. Sci Total Environ. 2022;806:150328. DOI:10.1016/j.scitotenv.2021.150328.

Wang C, Hou M, Shang K, Wang H, Wang J. Microplastics (polystyrene) exposure induces metabolic changes in the liver of rare minnow (Gobiocypris rarus). Molecules. 2022;27(3):584. DOI: 10.3390/molecules27030584.

Goodman KE, Hua T, Sang QX. Effects of polystyrene microplastics on human kidney and liver cell morphology, cellular proliferation, and metabolism. ACS Omega. 2022;7(38):34136-53. DOI: 10.1021/acsomega.2c03453.

Shengchen W, Jing L, Yujie Y, Yue W, Shiwen X. Polystyrene microplastics-induced ROS overproduction disrupts the skeletal muscle regeneration by converting myoblasts into adipocytes. J Hazard Mater. 2021;417:125962. DOI:10.1016/j.jhazmat.2021.125962.

Deng Y, Zhang Y, Qiao R, et al. Evidence that microplastics aggravate the toxicity of organophosphorus flame retardants in mice (Mus musculus). J Hazard Mater. 2018;357:348-54. DOI:10.1016/j.jhazmat.2018.06.017.

Jin Y, Lu L, Tu W, Luo T, Fu Z. Impacts of polystyrene microplastic on the gut barrier, microbiota and metabolism of mice. Sci Total Environ. 2019;649:308-17. DOI:10.1016/j.scitotenv.2018.08.353.

Lu L, Wan Z, Luo T, Fu Z, Jin Y. Polystyrene microplastics induce gut microbiota dysbiosis and hepatic lipid metabolism disorder in mice. Sci Total Enviorn. 2018;631:449-58. DOI:10.1016/j.scitotenv.2018.03.051.

Zheng H, Wang J, Wei X, Chang L, Liu S. Proinflammatory properties and lipid disturbance of polystyrene microplastics in the livers of mice with acute colitis. Sci Total Enviorn. 2021;750:143085. DOI: 10.1016/j.scitotenv.2020.143085.

Trinder P. Determination of blood glucose using an oxidase-peroxidase system with a non-carcinogenic chromogen. J Clin Pathol.1969; 22(2):158-61. DOI:10.1136/jcp.22.2.158.

Montgomery R. Determination of glycogen. Arch Biochem Biophys. 1957; 67:378–86. DOI:10.1016/0003-9861(57)90292-8.

Segal S, Blair AE, Wyngaarden JB. An enzymatic spectrophotometric method for the determination of pyruvic acid in blood. J Lab Clin Med. 1956; 48(1): 137–43. PMID: 13332352.

Rosen H. A modified ninhydrin colorimetric analysis for amino acids. Arch Biochem Biophys. 1957; 67(1):10-5. DOI:10.1016/0003-9861(57)90241-2.

Reitman S, Frankel S. A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am J Clin Pathol. 1957; 28(1):56-63. DOI:10.1093/ajcp/28.1.56.

Plummer DT. An introduction to practical biochemistry. New Delhi: Tata McGraw Hill, 1988: ed 3. p. 273. ISBN 978-0070994874

Hollywood KA, Shadi IT, Goodacre R. Monitoring the succinate dehydrogenase activity isolated from mitochondria by surface enhanced Raman scattering. J Phys Chem C. 2010;114(16):7308-13. DOI: 10.1021/jp908950x.

Bergmeyer HU, Gawehn K, Grassl M. Methods of enzymatic analysis. 1, Academic Press Inc; 1974:pp521-522.

Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193(1):265-75. PMID: 14907713.

Brun NR, van Hage P, Hunting ER. et al. Polystyrene nanoplastics disrupt glucose metabolism and cortisol levels with a possible link to behavioural changes in larval zebrafish. Commun Biol. 2019;2:382. DOI:10.1038/s42003-019-0629-6.

Sayeed A, Akhtar FM, Saleem A, Akhtar B, Sharif A. Reproductive and metabolic toxic effects of polystyrene microplastics in adult female Wistar rats: a mechanistic study. Environ Sci Pollut Res. 2023; 30: 63185-99. DOI:10.1007/s11356-023-26565-6.

Deng Y, Zhang Y, Lemos B, Ren H. Tissue accumulation of microplastics in mice and biomarker responses suggest widespread health risks of exposure. Sci Rep. 2017;7:46687. DOI:10.1038/srep46687.

Liang B, Huang Y, Zhong Y, et al. Brain single-nucleus transcriptomics highlights that polystyrene nanoplastics potentially induce Parkinson's disease-like neurodegeneration by causing energy metabolism disorders in mice. J Hazard Mater. 2022;430:128459. DOI:10.1016/j.jhazmat.2022.128459.