Debarati Roy, Mousumi Dutta, Mukti Mondal, Kaushik Sarkar, Goutam Paul*

 Molecular Neurotoxicology Laboratory, Department of Physiology,

University of Kalyani, Kalyani, Nadia-741235, West Bengal, India

*Corresponding author: goutampaul.ku@gmail.com

Received: May 31, 2021 / Revised: June 23, 2021/ Accepted: June 27, 2021 

Abstract

Bisphenol S (BPS) being a component of storage and packaging materials of foodstuffs, beverages and drinking water, contaminates them through BPS-leaching. BPS exposure to humans occurs predominantly through the consumption of BPS-intoxicated foodstuffs and subsequently BPS absorption through the small intestine into bloodstream. Though, the probable toxic effects of BPS on contractile function of small intestinal visceral smooth muscle (VSM) that provides motility to the small intestine, remains poorly understood. So, the present study aims to evaluate the effects of BPS on the efferent neurocrine mechanisms involved in the intrinsic rhythmic contraction of small intestinal VSM. Experiments were performed on duodenum segment of small intestine isolated from adult male Sprague-Dawley rats to examine the effects of BPS exposure on the movement of the duodenum, acetylcholinesterase (AChE) activity, levels of cellular oxidative stress biomarkers, and activities of cytosolic antioxidant enzymes at 100µM, 200µM, 400µM and 800µM doses of BPS for 1h duration ex vivo by using standard laboratory protocol. We observed significant decrease in frequency and amplitude of contraction of duodenum recorded ex vivo in single-dose acute exposure experiments in BPS-exposed groups compared to the control group (P<0.05). Besides, acetylcholinesterase (AChE) activity in duodenal homogenate has been increased significantly along with significant alterations in both the levels of oxidative stress biomarkers and activities of antioxidant enzymes in a dose-response manner in BPS-exposed groups (P<0.001). Our results indicate that BPS inhibits contraction of duodenal VSM probably by inhibiting the activity of excitatory cholinergic myenteric efferents through inducing enzymatic activity of AChE and promoting oxidative stress in duodenum.

Keywords Bisphenol S, Duodenal visceral smooth muscle, Cholinergic myenteric efferent, AChE activity, Oxidative stress

How to cite this article:

Roy, D., Dutta, M., Mondal, M., Sarkar, K., Paul, G. (2021). Effect of Bisphenol S (BPS) on the contraction of duodenal visceral smooth muscle ex vivo in rat. Science Archives, Vol.2(2),99-108. http://dx.doi.org/10.47587/SA.2021.2207

References

Andrews, J. M., & Blackshaw, L. A. (2010). Small intestinal motor and sensory function and dysfunction. In M. Feldman, L. S. Friedman & L. J. Brandt (Ed.), Sleisenger and Fordtran’s gastrointestinal and liver disease: Pathophysiology/diagnosis/management (pp. 1643-1658). Philadelphia: Saunders.

Ayala, A., Muñoz, M. F., & Argüelles, S. (2014). Lipid peroxidation: Production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Medicine and Cellular Longevity, 2014, 360438. https://doi.org/10.1155/2014/360438

Beers, R. F., & Sizer, I. W. (1952). A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. Journal of Biological Chemistry, 195(1), 133-140. https://doi.org/10.1016/S0021-9258(19)50881-X

Bousoumah, R., Leso, V., Iavicoli, I., Huuskonen, P., Viegas, S., Porras, S. P., Santonen, T., Frery, N., Robert, A., & Ndaw, S. (2021). Biomonitoring of occupational exposure to bisphenol A, bisphenol S and bisphenol F: A systematic review. Science of the Total Environment, 783, 146905. https://doi.org/10.1016/j.scitotenv.2021.146905

Buege, J. A., & Aust, S. D. (1978). Microsomal lipid peroxidation. In S. Fleischer & L. Packer (Ed.), Methods in enzymology, Biomembranes, Part C: Biological oxidations: Microsomal, cytochrome P450, and other hemoprotein systems (Vol. 52, pp. 302-310). New York: Academic Press. https://doi.org/10.1016/S0076-6879(78)52032-6

Caballero-Casero, N., Lunar, L., & Rubio, S. (2016). Analytical methods for the determination of mixtures of bisphenols and derivatives in human and environmental exposure sources and biological fluids. A review. Analytica Chimica Acta, 908, 22-53. https://doi.org/10.1016/j.aca.2015.12.034

Cao, P., Zhong, H., Qiu, K., Li, D., Wu, G., Sui, H., & Song, Y. (2021). Exposure to bisphenol A and its substitutes, bisphenol F and bisphenol S from canned foods and beverages on Chinese market. Food Control, 120, 107502. https://doi.org/10.1016/j.foodcont.2020.107502

Dutta, M. & Paul, G. (2019). Gallic acid protects rat liver mitochondria ex vivo from bisphenol A induced oxidative stress mediated damages. Toxicology Reports, 6, 578-589. https://doi.org/10.1016/j.toxrep.2019.06.011

Ellman, G. L., Courtney, K. D., Andres, V., & Featherstone, R. M. (1961). A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology, 7(2), 88-95. https://doi.org/10.1016/0006-2952(61)90145-9

Gonzalez, A., & Sarna, S. K. (2001). Different types of contractions in rat colon and their modulation by oxidative stress. American Journal of Physiology-Gastrointestinal and Liver Physiology, 280(4), G546-G554. https://doi.org/10.1152/ajpgi.2001.280.4.G546

Gupta, R., & Singh, K. K. (2007). Stability studies on a cough syrup in plastic containers. Indian Journal of Pharmaceutical Sciences, 69(3), 408-413. 10.4103/0250-474X.34551

Habig, W. H., Pabst, M. J., & Jakoby, W. B. (1974). Glutathione S-transferases the first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 249(22), 7130-7139. https://doi.org/10.1016/S0021-9258(19)42083-8

Hassan, Z. K., Elobeid, M. A., Virk, P., Omer, S. A., ElAmin, M., Daghestani, M. H., & AlOlayan, E. M. (2012). Bisphenol A induces hepatotoxicity through oxidative stress in rat model. Oxidative Medicine and Cellular Longevity, 2012, 194829. https://doi.org/10.1155/2012/194829

Ho, Y. S., Magnenat, J. L., Gargano, M., & Cao, J. (1998). The nature of antioxidant defense mechanisms: A lesson from transgenic studies. Environmental Health Perspectives, 106(Suppl 5), 1219-1228. https://doi.org/10.1289/ehp.98106s51219

Horan, T. S., Pulcastro, H., Lawson, C., Gerona, R., Martin, S., Gieske, M. C., Sartain, C. V., & Hunt, P. A. (2018). Replacement bisphenols adversely affect mouse gametogenesis with consequences for subsequent generations. Current Biology, 28(18), 2948-2954. https://doi.org/10.1016/j.cub.2018.06.070

Ijaz, S., Ullah, A., Shaheen, G., & Jahan, S. (2020). Exposure of BPA and its alternatives like BPB, BPF, and BPS impair subsequent reproductive potentials in adult female Sprague Dawley rats. Toxicology Mechanisms and Methods, 30(1), 60-72. https://doi.org/10.1080/15376516.2019.1652873

Khadrawy, Y. A., Nour, N. A., & Ezz, H. S. A. (2011). Effect of oxidative stress induced by paradoxical sleep deprivation on the activities of Na+, K+-ATPase and acetylcholinesterase in the cortex and hippocampus of rat. Translational Research-Journal of Laboratory and Clinical Medicine, 157(2), 100-107. https://doi.org/10.1016/j.trsl.2010.11.005

Khmiri, I., Côté, J., Mantha, M., Khemiri, R., Lacroix, M., Gely, C., Toutain, P., Picard-Hagen, N., Gayrard, V., & Bouchard, M. (2020). Toxicokinetics of bisphenol-S and its glucuronide in plasma and urine following oral and dermal exposure in volunteers for the interpretation of biomonitoring data. Environment International, 138, 105644. https://doi.org/10.1016/j.envint.2020.105644

Lehmler, H. J., Liu, B., Gadogbe, M., & Bao, W. (2018). Exposure to bisphenol A, bisphenol F, and bisphenol S in US adults and children: The national health and nutrition examination survey 2013–2014. ACS Omega, 3(6), 6523-6532. https://doi.org/10.1021/acsomega.8b00824

Lowry, O. H., Rosebrough, N. J., Farr, A. L., & Randall, R. J. (1951). Protein measurement with the folin phenol reagent. Journal of Biological Chemistry, 193, 265-275. https://doi.org/10.1016/S0021-9258(19)52451-6

Maćczak, A., Cyrkler, M., Bukowska, B., & Michałowicz, J. (2017). Bisphenol A, bisphenol S, bisphenol F and bisphenol AF induce different oxidative stress and damage in human red blood cells (in vitro study). Toxicology In Vitro, 41, 143-149. https://doi.org/10.1016/j.tiv.2017.02.018

Marklund, S., & Marklund, G. (1974). Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. European Journal of Biochemistry, 47(3), 469-474. https://doi.org/10.1111/j.1432-1033.1974.tb03714.x

Melo, J. B., Agostinho, P., & Oliveira, C. R. (2003). Involvement of oxidative stress in the enhancement of acetylcholinesterase activity induced by amyloid beta-peptide. Neuroscience Research, 45(1), 117-127. https://doi.org/10.1016/S0168-0102(02)00201-8

Moreira, E. L. G., de Oliveira, J., Nunes, J. C., Santos, D. B., Nunes, F. C., Vieira, D. S. C., Ribeiro-do-Valle, R. M., Pamplona, F. A., de Bem, A. F., Farina, M., Walz, R., & Prediger, R. D. (2012). Age-related cognitive decline in hypercholesterolemic LDL receptor knockout mice (LDLr−/−): Evidence of antioxidant imbalance and increased acetylcholinesterase activity in the prefrontal cortex. Journal of Alzheimer’s Disease, 32(2), 495-511. https://doi.org/10.3233/JAD-2012-120541

Paglia, D. E., & Valentine, W. N. (1967). Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. Translational Research-Journal of Laboratory and Clinical Medicine, 70(1), 158-169. https://doi.org/10.5555/uri:pii:0022214367900765

Quinn, D. M. (1987). Acetylcholinesterase: Enzyme structure, reaction dynamics, and virtual transition states. Chemical Reviews, 87(5), 955-979. https://doi.org/10.1021/cr00081a005

Sabry, R., Saleh, A. C., Stalker, L., LaMarre, J., & Favetta, L. A. (2021). Effects of bisphenol A and bisphenol S on microRNA expression during bovine (Bos taurus) oocyte maturation and early embryo development. Reproductive Toxicology, 99, 96-108. https://doi.org/10.1016/j.reprotox.2020.12.001

Salahinejad, A., Attaran, A., Naderi, M., Meuthen, D., Niyogi, S., & Chivers, D. P. (2021). Chronic exposure to bisphenol S induces oxidative stress, abnormal anxiety, and fear responses in adult zebrafish (Danio rerio). Science of the Total Environment, 750, 141633. https://doi.org/10.1016/j.scitotenv.2020.141633

Sarkar, K., Tarafder, P., Nath, P. P., & Paul, G. (2013). Bisphenol A inhibits duodenal movement in rat by increasing acetylcholinesterase activity and decreasing availability of free Ca2+ in smooth muscle cells. International Journal of Pharma and Bio Sciences, 4(2), B679-B688.

Sarkar, K., Tarafder, P., & Paul, G. (2016). Bisphenol A inhibits duodenal movement ex vivo of rat through nitric oxide-mediated soluble guanylyl cyclase and α-adrenergic signaling pathways. Journal of Applied Toxicology, 36(1), 131-139. https://doi.org/10.1002/jat.3154

Sedlak, J., & Lindsay, R. H. (1968). Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Analytical Biochemistry, 25, 192-205. https://doi.org/10.1016/0003-2697(68)90092-4

Shi, X. Z., Lindholm, P. F., & Sarna, S. K. (2003). NF-κB activation by oxidative stress and inflammation suppresses contractility in colonic circular smooth muscle cells. Gastroenterology, 124(5), 1369-1380. https://doi.org/10.1016/S0016-5085(03)00263-4

Staal, G. E. J., Visser, J., & Veeger, C. (1969). Purification and properties of glutathione reductase of human erythrocytes. Biochimica et Biophysica Acta (BBA)-Enzymology, 185(1), 39-48. https://doi.org/10.1016/0005-2744(69)90280-0

Ullah, A., Pirzada, M., Jahan, S., Ullah, H., & Khan, M. J. (2019). Bisphenol A analogues bisphenol B, bisphenol F, and bisphenol S induce oxidative stress, disrupt daily sperm production, and damage DNA in rat spermatozoa: a comparative in vitro and in vivo study. Toxicology and Industrial Health, 35(4), 294-303. https://doi.org/10.1177/0748233719831528

Ullah, H., Jahan, S., Ain, Q. U., Shaheen, G., & Ahsan, N. (2016). Effect of bisphenol S exposure on male reproductive system of rats: A histological and biochemical study. Chemosphere, 152, 383-391. https://doi.org/10.1016/j.chemosphere.2016.02.125

Van der Vliet, A., Tuinstra, T. J., & Bast, A. (1989). Modulation of oxidative stress in the gastrointestinal tract and effect on rat intestinal motility. Biochemical Pharmacology, 38(17), 2807-2818. https://doi.org/10.1016/0006-2952(89)90435-8

Vona, R., Pallotta, L., Cappelletti, M., Severi, C., & Matarrese, P. (2021). The impact of oxidative stress in human pathology: Focus on gastrointestinal disorders. Antioxidants, 10(2), 201. https://doi.org/10.3390/antiox10020201

Yang, Y., Yu, J., Yin, J., Shao, B., & Zhang, J. (2014). Molecularly imprinted solid-phase extraction for selective extraction of bisphenol analogues in beverages and canned food. Journal of Agricultural and Food Chemistry, 62(46), 11130-11137. https://doi.org/10.1021/jf5037933

Zhang, R., Liu, R., & Zong, W. (2016). Bisphenol S interacts with catalase and induces oxidative stress in mouse liver and renal cells. Journal of Agricultural and Food Chemistry, 64(34), 6630-6640. https://doi.org/10.1021/acs.jafc.6b02656

Zhang, Z., Lin, L., Gai, Y., Hong, Y., Li, L., & Weng, L. (2018). Subchronic bisphenol S exposure affects liver function in mice involving oxidative damage. Regulatory Toxicology and Pharmacology, 92, 138-144. https://doi.org/10.1016/j.yrtph.2017.11.018

License                      Article Metadata

This work is licensed under a Creative Commons Attribution 4.0 International License.

View Details