The Influence of Bisphenol A (BPA) on the Occurrence of Selected Active Substances in Neuregulin 1 (NRG1)-Positive Enteric Neurons in the Porcine Large Intestine

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2021 Oct 13

PMID 34638647

Citations 5

Authors

Krystyna Makowska

Kamila Szymanska

Jaroslaw Calka

Slawomir Gonkowski

Affiliations

Soon will be listed here.

Abstract

Bisphenol A (BPA) is a substance used in the manufacture of plastics which shows multidirectional adverse effects on living organisms. Since the main path of intoxication with BPA is via the gastrointestinal (GI) tract, the stomach and intestine are especially vulnerable to the impact of this substance. One of the main factors participating in the regulation of intestinal functions is the enteric nervous system (ENS), which is characterized by high neurochemical diversity. Neuregulin 1 (NRG1) is one of the lesser-known active substances in the ENS. During the present study (performed using the double immunofluorescence method), the co-localization of NRG1 with other neuronal substances in the ENS of the caecum and the ascending and descending colon has been investigated under physiological conditions and after the administration of BPA. The obtained results indicate that NRG1-positive neurons also contain substance P, vasoactive intestinal polypeptide, a neuronal isoform of nitric oxide synthase and galanin and the degree of each co-localization depend on the type of enteric plexus and the particular fragment of the intestine. Moreover, it has been shown that BPA generally increases the degree of co-localization of NRG1 with other substances.

Citing Articles

Distribution and neurochemical characterisation of neurons containing neuregulin 1 in the enteric nervous system within the porcine small intestine.

Puchala L, Gonkowski S, Rytel L, Wojtkiewicz J, Grzegorzewski W J Vet Res. 2025; 68(4):623-632.

PMID: 39776680 PMC: 11702255. DOI: 10.2478/jvetres-2024-0063.

Bisphenol A-What Do We Know? A Global or Local Approach at the Public Health Risk Level.

Charkiewicz A, Omeljaniuk W, Niklinski J Int J Mol Sci. 2024; 25(11).

PMID: 38892416 PMC: 11172700. DOI: 10.3390/ijms25116229.

Neuregulin 1 (NRG1) and its receptors in the enteric nervous system and other parts of the gastrointestinal wall.

Gonkowski S Histol Histopathol. 2024; 39(9):1089-1099.

PMID: 38407437 DOI: 10.14670/HH-18-721.

Protective Effects of Selenium Nanoparticles against Bisphenol A-Induced Toxicity in Porcine Intestinal Epithelial Cells.

Pan Z, Huang J, Hu T, Zhang Y, Zhang L, Zhang J Int J Mol Sci. 2023; 24(8).

PMID: 37108405 PMC: 10139072. DOI: 10.3390/ijms24087242.

The Comparison of the Influence of Bisphenol A (BPA) and Its Analogue Bisphenol S (BPS) on the Enteric Nervous System of the Distal Colon in Mice.

Makowska K, Lepiarczyk E, Gonkowski S Nutrients. 2023; 15(1).

PMID: 36615857 PMC: 9824883. DOI: 10.3390/nu15010200.

References

Lordal M, Theodorsson E, Hellstrom P . Tachykinins influence interdigestive rhythm and contractile strength of human small intestine. Dig Dis Sci. 1997; 42(9):1940-9. DOI: 10.1023/a:1018875529739. View

Szymanska K, Makowska K, Calka J, Gonkowski S . The Endocrine Disruptor Bisphenol A (BPA) Affects the Enteric Neurons Immunoreactive to Neuregulin 1 (NRG1) in the Enteric Nervous System of the Porcine Large Intestine. Int J Mol Sci. 2020; 21(22). PMC: 7699376. DOI: 10.3390/ijms21228743. View

McDonald T, Cipris S, Woskowska Z, Daniel E . Galanin inhibition of vasoactive intestinal polypeptide release and circular muscle motility in the isolated perfused canine ileum. Gastroenterology. 1991; 101(6):1471-6. DOI: 10.1016/0016-5085(91)90381-t. View

Geuna S, Tos P, Raimondo S, Lee J, Gambarotta G, Nicolino S . Functional, morphological and biomolecular assessment of posttraumatic neuro-muscular recovery in the rat forelimb model. Acta Neurochir Suppl. 2007; 100:173-7. DOI: 10.1007/978-3-211-72958-8_36. View

Filpa V, Carpanese E, Marchet S, Pirrone C, Conti A, Rainero A . Nitric oxide regulates homeoprotein OTX1 and OTX2 expression in the rat myenteric plexus after intestinal ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol. 2017; 312(4):G374-G389. DOI: 10.1152/ajpgi.00386.2016. View

Makowska K . Chemically induced inflammation and nerve damage affect the distribution of vasoactive intestinal polypeptide-like immunoreactive (VIP-LI) nervous structures in the descending colon of the domestic pig. Neurogastroenterol Motil. 2018; 30(11):e13439. DOI: 10.1111/nmo.13439. View

Zhao W . The expression and localization of neuregulin-1 (Nrg1) in the gastrointestinal system of the rhesus monkey. Folia Histochem Cytobiol. 2013; 51(1):38-44. DOI: 10.5603/FHC.2013.006. View

Sussman C, Vartanian T, Miller R . The ErbB4 neuregulin receptor mediates suppression of oligodendrocyte maturation. J Neurosci. 2005; 25(24):5757-62. PMC: 6724872. DOI: 10.1523/JNEUROSCI.4748-04.2005. View

Bulc M, Gonkowski S, Landowski P, Kaminska B, Calka J . Immunohistochemical distribution of cocaine and amphetamine regulatory peptide-like immunoreactive (CART-LI) nerve fibers in the circular muscle layer and their relationship to other peptides in the human caecum. Acta Histochem. 2014; 116(6):1029-36. DOI: 10.1016/j.acthis.2014.04.009. View

10.

Espinosa-Medina I, Jevans B, Boismoreau F, Chettouh Z, Enomoto H, Muller T . Dual origin of enteric neurons in vagal Schwann cell precursors and the sympathetic neural crest. Proc Natl Acad Sci U S A. 2017; 114(45):11980-11985. PMC: 5692562. DOI: 10.1073/pnas.1710308114. View

11.

Cordero-Llana O, Rinaldi F, Brennan P, Wynick D, Caldwell M . Galanin promotes neuronal differentiation from neural progenitor cells in vitro and contributes to the generation of new olfactory neurons in the adult mouse brain. Exp Neurol. 2014; 256:93-104. DOI: 10.1016/j.expneurol.2014.04.001. View

12.

Qu W, Zhao Z, Chen S, Zhang L, Wu D, Chen Z . Bisphenol A suppresses proliferation and induces apoptosis in colonic epithelial cells through mitochondrial and MAPK/AKT pathways. Life Sci. 2018; 208:167-174. DOI: 10.1016/j.lfs.2018.07.040. View

13.

Verma N, Rettenmeier A, Schmitz-Spanke S . Recent advances in the use of Sus scrofa (pig) as a model system for proteomic studies. Proteomics. 2011; 11(4):776-93. DOI: 10.1002/pmic.201000320. View

14.

Zhao Z, Qu W, Wang K, Chen S, Zhang L, Wu D . Bisphenol A inhibits mucin 2 secretion in intestinal goblet cells through mitochondrial dysfunction and oxidative stress. Biomed Pharmacother. 2019; 111:901-908. DOI: 10.1016/j.biopha.2019.01.007. View

15.

Anselmi L, Stella Jr S, Lakhter A, Hirano A, Tonini M, Sternini C . Galanin receptors in the rat gastrointestinal tract. Neuropeptides. 2005; 39(3):349-52. PMC: 3846504. DOI: 10.1016/j.npep.2004.12.023. View

16.

Vasina V, Barbara G, Talamonti L, Stanghellini V, Corinaldesi R, Tonini M . Enteric neuroplasticity evoked by inflammation. Auton Neurosci. 2006; 126-127:264-72. DOI: 10.1016/j.autneu.2006.02.025. View

17.

Piqueras L, Tache Y, Martinez V . Galanin inhibits gastric acid secretion through a somatostatin-independent mechanism in mice. Peptides. 2004; 25(8):1287-95. DOI: 10.1016/j.peptides.2004.06.003. View

18.

Shimizu Y, Matsuyama H, Shiina T, Takewaki T, Furness J . Tachykinins and their functions in the gastrointestinal tract. Cell Mol Life Sci. 2007; 65(2):295-311. PMC: 11131725. DOI: 10.1007/s00018-007-7148-1. View

19.

Vota D, Aguero M, Grasso E, Hauk V, Gallino L, Soczewski E . Progesterone and VIP cross-talk enhances phagocytosis and anti-inflammatory profile in trophoblast-derived cells. Mol Cell Endocrinol. 2017; 443:146-154. DOI: 10.1016/j.mce.2017.01.022. View

20.

Viehover A, Miller R, Park S, Fischbach G, Vartanian T . Neuregulin: an oligodendrocyte growth factor absent in active multiple sclerosis lesions. Dev Neurosci. 2002; 23(4-5):377-86. DOI: 10.1159/000048721. View