Skip to main content

Advertisement

SpringerLink
Log in

Bisphenol A Regulates the TNFR1 Pathway and Excessive ROS Mediated by miR-26a-5p/ADAM17 Axis to Aggravate Selenium Deficiency-Induced Necroptosis in Broiler Veins

  • Research
  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Selenium (Se) deficiency can affect the expression of microRNA (miRNA) and induce necroptosis, apoptosis, etc., resulting in damage to various tissues and organs. Bisphenol A (BPA) exposure can cause adverse consequences such as oxidative stress, endothelial dysfunction, and atherosclerosis. The toxic effects of combined treatment with Se-deficiency and BPA exposure may have a synergistic effect. We replicated the BPA exposure and Se-deficiency model in broiler to investigate whether the combined treatment of Se-deficiency and BPA exposure induced necroptosis and inflammation of chicken vascular tissue via the miR-26A-5p/ADAM17 axis. We found that Se deficiency and BPA exposure significantly inhibited the expression of miR-26a-5p and increased the expression of ADAM17, thereby increasing reactive oxygen species (ROS) production. Subsequently, we discovered that the tumor necrosis factor receptor (TNFR1), which was highly expressed, activated the necroptosis pathway through receptor-interacting protein kinase 1 (RIPK1), receptor-interacting protein kinase 3 (RIPK3), and mixed-lineage kinase domain-like (MLKL), and regulated the heat shock proteins-related genes expressions and inflammation-related genes expressions after exposure to BPA and selenium deficiency. In vitro, we found that miR-26a-5p knockdown and increased ADAM17 can induce necroptosis by activating the TNFR1 pathway. Similarly, both N-Acetyl-L-cysteine (NAC), Necrostatin-1 (Nec-1), and miR-26a-5p mimic prevented necroptosis and inflammation caused by BPA exposure and Se deficiency. These results suggest that BPA exposure activates the miR-26a-5p/ADAM17 axis and exacerbates Se deficient-induced necroptosis and inflammation through the TNFR1 pathway and excess ROS. This study lays a data foundation for future ecological and health risk assessments of nutrient deficiencies and environmental toxic pollution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data Availability

The raw data supporting the conclusions of this manuscript will be made available by the authors, without undue reservation, to any qualified researcher.

References

  1. Yamazaki E, Yamashita N, Taniyasu S, Lam J, Lam PK, Moon HB et al (2015) Bisphenol A and other bisphenol analogues including BPS and BPF in surface water samples from Japan, China. Korea and India Ecotoxicol Environ Saf 122:565–572. https://doi.org/10.1016/j.ecoenv.2015.09.029

    Article  CAS  PubMed  Google Scholar 

  2. Yan Z, Liu Y, Yan K, Wu S, Han Z, Guo R et al (2017) Bisphenol analogues in surface water and sediment from the shallow Chinese freshwater lakes: occurrence, distribution, source apportionment, and ecological and human health risk. Chemosphere 184:318–328. https://doi.org/10.1016/j.chemosphere.2017.06.010

    Article  ADS  CAS  PubMed  Google Scholar 

  3. Friques AGF, Santos FDN, Angeli DB, Silva FAC, Dias AT, Aires R et al (2020) Bisphenol 4A contamination in infant rats: molecular, structural, and physiological cardiovascular changes and the protective role of kefir. J Nutr Biochem 75:108254. https://doi.org/10.1016/j.jnutbio.2019.108254

    Article  CAS  PubMed  Google Scholar 

  4. Jones DC, Miller GW (2008) The effects of environmental neurotoxicants on the dopaminergic system: a possible role in drug addiction. Biochem Pharmacol 76:569–581. https://doi.org/10.1016/j.bcp.2008.05.010

    Article  CAS  PubMed  Google Scholar 

  5. Ziv-Gal A, Flaws JA (2016) Evidence for bisphenol A-induced female infertility: a review (2007–2016). Fertil Steril 106:827–856. https://doi.org/10.1016/j.fertnstert.2016.06.027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Wan MLY, Co VA, El-Nezami H (2022) Endocrine disrupting chemicals and breast cancer: a systematic review of epidemiological studies. Crit Rev Food Sci Nutr 62:6549–6576

  7. Frat L, Chertemps T, Pesce E, Bozzolan F, Dacher M, Planello R et al (2023) Impact of single and combined exposure to priority pollutants on gene expression and post-embryonic development in Drosophila melanogaster. Ecotoxicol Environ Saf. 250:114491. https://doi.org/10.1016/j.ecoenv.2022.114491

    Article  CAS  PubMed  Google Scholar 

  8. Azizidoost S, Nasrolahi A, Sheykhi-Sabzehpoush M, Akiash N, Assareh AR, Anbiyaee O et al (2023) Potential roles of endothelial cells-related non-coding RNAs in cardiovascular diseases. Pathol Res Pract. 242:154330. https://doi.org/10.1016/j.prp.2023.154330

    Article  CAS  PubMed  Google Scholar 

  9. Kong B, Qin Z, Ye Z, Yang X, Li L, Su Q (2019) microRNA-26a-5p affects myocardial injury induced by coronary microembolization by modulating HMGA1. J Cell Biochem 120:10756–10766. https://doi.org/10.1002/jcb.28367

    Article  CAS  PubMed  Google Scholar 

  10. Han G, Li H, Guo H, Yi C, Yu B, Lin Y et al (2022) The roles and mechanisms of miR-26 derived from exosomes of adipose-derived stem cells in the formation of carotid atherosclerotic plaque. Ann Transl Med 10:1134. https://doi.org/10.1134/10.21037/atm-22-4247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Yu X, Mao M, Liu X, Shen T, Li T, Yu H et al (2020) A cytosolic heat shock protein 90 and co-chaperone p23 complex activates RIPK3/MLKL during necroptosis of endothelial cells in acute respiratory distress syndrome. J Mol Med (Berl) 98:569–583. https://doi.org/10.1007/s00109-020-01886-y

    Article  CAS  PubMed  Google Scholar 

  12. Zhang W, Sun X, Lei Y, Liu X, Zhang Y, Wang Y et al (2023) Roles of selenoprotein K in oxidative stress and endoplasmic reticulum stress under selenium deficiency in chicken liver. Comp Biochem Physiol C Toxicol Pharmacol. 264:109504. https://doi.org/10.1016/j.cbpc.2022.109504

    Article  CAS  PubMed  Google Scholar 

  13. Kanazawa J, Kakisaka K, Suzuki Y, Yonezawa T, Abe H, Wang T et al (2022) Excess fructose enhances oleatic cytotoxicity via reactive oxygen species production and causes necroptosis in hepatocytes. J Nutr Biochem. 107:109052. https://doi.org/10.1016/j.jnutbio.2022.109052

    Article  CAS  PubMed  Google Scholar 

  14. Du Q, Yao H, Yao L, Zhang Z, Lei X, Xu S (2016) Selenium deficiency influences the expression of selenoproteins and inflammatory cytokines in chicken aorta vessels. Biol Trace Elem Res 173:501–513. https://doi.org/10.1007/s12011-016-0676-5

    Article  CAS  PubMed  Google Scholar 

  15. Pan T, Hu X, Liu T, Xu Z, Wan N, Zhang Y et al (2018) MiR-128-1-5p regulates tight junction induced by selenium deficiency via targeting cell adhesion molecule 1 in broilers vein endothelial cells. J Cell Physiol 233:8802–8814. https://doi.org/10.1002/jcp.26794

    Article  CAS  PubMed  Google Scholar 

  16. Miyazaki K, Watanabe C, Mori K, Yoshida K, Ohtsuka R (2005) The effects of gestational arsenic exposure and dietary selenium deficiency on selenium and selenoenzymes in maternal and fetal tissues in mice. Toxicology 208:357–365. https://doi.org/10.1016/j.tox.2004.11.030

    Article  CAS  PubMed  Google Scholar 

  17. Carmean CM, Mimoto M, Landeche M, Ruiz D, Chellan B, Zhao L et al (2021) Dietary selenium deficiency partially mimics the metabolic effects of arsenic. Nutrients 13. https://doi.org/10.3390/nu13082894

  18. Zheng Y, Guan H, Yang J, Cai J, Liu Q, Zhang Z (2021) Calcium overload and reactive oxygen species accumulation induced by selenium deficiency promote autophagy in swine small intestine. Anim Nutr 7:997–1008. https://doi.org/10.1016/j.aninu.2021.05.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Du Y, Xu T, Luo D, Wang Y, Yin H, Liu C et al (2023) Perfluorooctane sulfonate-induced apoptosis in kidney cells by triggering the NOX4/ROS/JNK axis and antagonism of cannabidiol. Environ Toxicol. https://doi.org/10.1002/tox.23794

    Article  PubMed  Google Scholar 

  20. Wang X, Xu T, Luo D, Li S, Tang X, Ding J et al (2023) Cannabidiol alleviates perfluorooctanesulfonic acid-induced cardiomyocyte apoptosis by maintaining mitochondrial dynamic balance and energy metabolic homeostasis. J Agric Food Chem 71:5450–5462. https://doi.org/10.1021/acs.jafc.2c08378

    Article  CAS  PubMed  Google Scholar 

  21. Lei Y, Zhang W, Gao M, Lin H (2023) Mechanism of evodiamine blocking Nrf2/MAPK pathway to inhibit apoptosis of grass carp hepatocytes induced by DEHP. Comp Biochem Physiol C Toxicol Pharmacol. 263:109506. https://doi.org/10.1016/j.cbpc.2022.109506

    Article  CAS  PubMed  Google Scholar 

  22. Cai J, Huang J, Yang J, Chen X, Zhang H, Zhu Y et al (2022) The protective effect of selenoprotein M on non-alcoholic fatty liver disease: the role of the AMPKα1-MFN2 pathway and Parkin mitophagy. Cell Mol Life Sci 79:354. https://doi.org/10.1007/s00018-022-04385-0

    Article  CAS  PubMed  Google Scholar 

  23. Chen L, Tao D, Qi M, Wang T, Jiang Z, Xu S (2022) Cineole alleviates the BPA-inhibited NETs formation by regulating the p38 pathway-mediated programmed cell death. Ecotoxicol Environ Saf. 237:113558. https://doi.org/10.1016/j.ecoenv.2022.113558

    Article  CAS  PubMed  Google Scholar 

  24. Zhang Y, Xu Y, Chen B, Zhao B, Gao XJ (2022) Selenium deficiency promotes oxidative stress-induced mastitis via activating the NF-κB and MAPK pathways in dairy cow. Biol Trace Elem Res 200:2716–2726. https://doi.org/10.1007/s12011-021-02882-0

    Article  CAS  PubMed  Google Scholar 

  25. Elswefy SE, Abdallah FR, Atteia HH, Wahba AS, Hasan RA (2016) Inflammation, oxidative stress and apoptosis cascade implications in bisphenol A-induced liver fibrosis in male rats. Int J Exp Pathol 97:369–379. https://doi.org/10.1111/iep.12207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Aboul Ezz HS, Khadrawy YA, Mourad IM (2015) The effect of bisphenol A on some oxidative stress parameters and acetylcholinesterase activity in the heart of male albino rats. Cytotechnology 67:145–155. https://doi.org/10.1007/s10616-013-9672-1

    Article  CAS  PubMed  Google Scholar 

  27. Hasuoka PE, Iglesias JP, Teves M, Kaplan MM, Ferrúa NH, Pacheco PH (2021) Selenomethionine administration decreases the oxidative stress induced by post mortem ischemia in the heart, liver and kidneys of rats. Biometals 34:831–840. https://doi.org/10.1007/s10534-021-00310-3

    Article  CAS  PubMed  Google Scholar 

  28. Piao X, Liu Z, Li Y, Yao D, Sun L, Wang B et al (2019) Investigation of the effect for bisphenol A on oxidative stress in human hepatocytes and its interaction with catalase. Spectrochim Acta A Mol Biomol Spectrosc. 221:117149. https://doi.org/10.1016/j.saa.2019.117149

    Article  CAS  PubMed  Google Scholar 

  29. Jung J, Kim Y, Na J, Qiao L, Bang J, Kwon D et al (2021) Constitutive oxidative stress by SEPHS1 deficiency induces endothelial cell dysfunction. Int J Mol Sci 22:11646. https://doi.org/10.3390/ijms222111646

  30. Andersson H, Brittebo E (2012) Proangiogenic effects of environmentally relevant levels of bisphenol A in human primary endothelial cells. Arch Toxicol 86:465–474. https://doi.org/10.1007/s00204-011-0766-2

    Article  CAS  PubMed  Google Scholar 

  31. Siamwala JH, Dias PM, Majumder S, Joshi MK, Sinkar VP, Banerjee G et al (2013) L-theanine promotes nitric oxide production in endothelial cells through eNOS phosphorylation. J Nutr Biochem 24:595–605. https://doi.org/10.1016/j.jnutbio.2012.02.016

    Article  CAS  PubMed  Google Scholar 

  32. Easson S, Singh RD, Connors L, Scheidl T, Baker L, Jadli A et al (2022) Exploring oxidative stress and endothelial dysfunction as a mechanism linking bisphenol S exposure to vascular disease in human umbilical vein endothelial cells and a mouse model of postnatal exposure. Environ Int 170:107603. https://doi.org/10.1016/j.envint.2022.107603

    Article  CAS  PubMed  Google Scholar 

  33. Farah C, Michel LYM, Balligand JL (2018) Nitric oxide signalling in cardiovascular health and disease. Nat Rev Cardiol 15:292–316. https://doi.org/10.1038/nrcardio.2017.224

    Article  CAS  PubMed  Google Scholar 

  34. Mohsenzadeh MS, Razavi BM, Imenshahidi M, Mohajeri SA, Rameshrad M, Hosseinzadeh H (2021) Evaluation of green tea extract and epigallocatechin gallate effects on bisphenol A-induced vascular toxicity in isolated rat aorta and cytotoxicity in human umbilical vein endothelial cells. Phytother Res 35:996–1009. https://doi.org/10.1002/ptr.6861

    Article  CAS  PubMed  Google Scholar 

  35. Reventun P, Sanchez-Esteban S, Cook A, Cuadrado I, Roza C, Moreno-Gomez-Toledano R et al (2020) Bisphenol A induces coronary endothelial cell necroptosis by activating RIP3/CamKII dependent pathway. Sci Rep 10:4190. https://doi.org/10.1038/s41598-020-61014-1

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  36. Liu J, Chen T, Wang S, Wu H, Xu S (2022) BPA exposure aggravates necroptosis of myocardial tissue in selenium deficient broilers through NO-dependent endoplasmic reticulum stress. Toxicology. 472:153190. https://doi.org/10.1016/j.tox.2022.153190

    Article  CAS  PubMed  Google Scholar 

  37. Cui J, Liu H, Xu S (2020) Selenium-deficient diet induces necroptosis in the pig brain by activating TNFR1 via mir-29a-3p. Metallomics 12:1290–1301. https://doi.org/10.1039/d0mt00032a

    Article  CAS  PubMed  Google Scholar 

  38. Qin D, Wang X, Li Y, Yang L, Wang R, Peng J et al (2016) MicroRNA-223-5p and -3p cooperatively suppress necroptosis in ischemic/reperfused hearts. J Biol Chem 291:20247–20259. https://doi.org/10.1074/jbc.M116.732735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Yu Y, Chen M, Guo Q, Shen L, Liu X, Pan J et al (2023) Human umbilical cord mesenchymal stem cell exosome-derived miR-874-3p targeting RIPK1/PGAM5 attenuates kidney tubular epithelial cell damage. Cell Mol Biol Lett 28:12. https://doi.org/10.1186/s11658-023-00425-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Dou X, Yu X, Du S, Han Y, Li L, Zhang H et al (2022) Interferon-mediated repression of miR-324–5p potentiates necroptosis to facilitate antiviral defense. EMBO Rep. 23:e54438. https://doi.org/10.15252/embr.202154438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Bolik J, Krause F, Stevanovic M, Gandraß M, Thomsen I, Schacht SS et al (2022) Inhibition of ADAM17 impairs endothelial cell necroptosis and blocks metastasis. J Exp Med 219:e20201039. https://doi.org/10.1084/jem.20201039

  42. Cao C, Chen S, Song Z, Liu Z, Zhang M, Ma Z, et al. (2022) Inflammatory stimulation mediates nucleus pulposus cell necroptosis through mitochondrial function disfunction and oxidative stress pathway. Front Biosci (Landmark Ed). 27:111. https://doi.org/10.31083/j.fbl2704111

  43. Xue F, Cheng J, Liu Y, Cheng C, Zhang M, Sui W et al (2022) Cardiomyocyte-specific knockout of ADAM17 ameliorates left ventricular remodeling and function in diabetic cardiomyopathy of mice. Signal Transduct Target Ther 7:259. https://doi.org/10.1038/s41392-022-01054-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Mázló A, Jenei V, Burai S, Molnár T, Bácsi A, Koncz G (2022) Types of necroinflammation, the effect of cell death modalities on sterile inflammation. Cell Death Dis 13:423. https://doi.org/10.1038/s41419-022-04883-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Xu T, Liu Q, Chen D, Liu Y (2022) Atrazine exposure induces necroptosis through the P450/ROS pathway and causes inflammation in the gill of common carp (Cyprinus carpioL.). Fish Shellfish Immunol 131:809–816. https://doi.org/10.1016/j.fsi.2022.10.022

    Article  CAS  PubMed  Google Scholar 

  46. Carper SW, Duffy JJ, Gerner EW (1987) Heat shock proteins in thermotolerance and other cellular processes. Cancer Res 47:5249–5255

    CAS  PubMed  Google Scholar 

  47. Sidera K, Patsavoudi E (2014) HSP90 inhibitors: current development and potential in cancer therapy. Recent Pat Anticancer Drug Discov 9:1–20

    Article  CAS  PubMed  Google Scholar 

  48. Zhao XM, Chen Z, Zhao JB, Zhang PP, Pu YF, Jiang SH et al (2016) Hsp90 modulates the stability of MLKL and is required for TNF-induced necroptosis. Cell Death Dis 7:e2089. https://doi.org/10.1038/cddis.2015.390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Marunouchi T, Nishiumi C, Iinuma S, Yano E, Tanonaka K (2021) Effects of Hsp90 inhibitor on the RIP1-RIP3-MLKL pathway during the development of heart failure in mice. Eur J Pharmacol 898:173987. https://doi.org/10.1016/j.ejphar.2021.173987

    Article  CAS  PubMed  Google Scholar 

  50. Xue Y, Wang H, Tian B, Wang S, Gao XJ (2023) Selenium deficiency promotes the expression of LncRNA-MORC3, activating NLRP3-caspase-1/IL-1β signaling to induce inflammatory damage and disrupt tight junctions in piglets. Biol Trace Elem Res 201:2365–2376. https://doi.org/10.1007/s12011-022-03341-0

    Article  CAS  PubMed  Google Scholar 

  51. Billack B, Heck DE, Mariano TM, Gardner CR, Sur R, Laskin DL et al (2002) Induction of cyclooxygenase-2 by heat shock protein 60 in macrophages and endothelial cells. Am J Physiol Cell Physiol 283:C1267-1277. https://doi.org/10.1152/ajpcell.00609.2001

    Article  CAS  PubMed  Google Scholar 

  52. Khoso PA, Liu C, Liu C, Khoso MH, Li S (2016) Selenium deficiency activates heat shock protein expression in chicken spleen and thymus. Biol Trace Elem Res 173:492–500. https://doi.org/10.1007/s12011-016-0673-8

    Article  CAS  PubMed  Google Scholar 

  53. Kipp AP, Banning A, van Schothorst EM, Méplan C, Coort SL, Evelo CT et al (2012) Marginal selenium deficiency down-regulates inflammation-related genes in splenic leukocytes of the mouse. J Nutr Biochem 23:1170–1177. https://doi.org/10.1016/j.jnutbio.2011.06.011

    Article  CAS  PubMed  Google Scholar 

  54. Gu X, Wang Y, He Y, Zhao B, Zhang Q, Li S (2022) MiR-1656 targets GPX4 to trigger pyroptosis in broilers kidney tissues by activating NLRP3 inflammasome under Se deficiency. J Nutr Biochem. 105:109001. https://doi.org/10.1016/j.jnutbio.2022.109001

    Article  CAS  PubMed  Google Scholar 

  55. Migliaccio S, Bimonte VM, Besharat ZM, Sabato C, Lenzi A, Crescioli C et al (2021) Environmental contaminants acting as endocrine disruptors modulate atherogenic processes: new risk factors for cardiovascular diseases in women? Biomolecules 12:44. https://doi.org/10.3390/biom12010044

Download references

Acknowledgements

The authors thank the Key Laboratory of the Provincial Education Department of Heilongjiang for Common Animal Disease Prevention and Treatment, College of Veterinary Medicine, Northeast Agricultural University for providing conditions.

Funding

This work was supported by the Natural Science Foundation of Heilongjiang Province (ZD2022C005) and the National Natural Science Foundation (Grant No. 32072811).

Author information

Authors and Affiliations

  1. College of Veterinary Medicine, Northeast Agricultural University, Harbin, 150030, People’s Republic of China

    Xue Fan, Yixuan Wang, Jintao Zhang, Hongjin Lin & Shu Li

  2. School of Basic Medical Sciences, Youjiang Medical University for Nationalities, Baise, 533000, China

    Zhikun Bai

Authors
  1. Xue Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yixuan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jintao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hongjin Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhikun Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Xue Fan, Yixuan Wang, and Jintao Zhang. Supervision and software were performed by Hongjin Lin. Reviewing, editing, and funding acquisition were performed by Zhikun Bai and Shu Li. The first draft of the manuscript was written by Xue Fan, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Zhikun Bai or Shu Li.

Ethics declarations

Ethics Approval

All procedures used in this study were approved by the Institutional Animal Care and Use Committee (NEAUEC20200311) of Northeast Agricultural University.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fan, X., Wang, Y., Zhang, J. et al. Bisphenol A Regulates the TNFR1 Pathway and Excessive ROS Mediated by miR-26a-5p/ADAM17 Axis to Aggravate Selenium Deficiency-Induced Necroptosis in Broiler Veins. Biol Trace Elem Res 202, 1722–1740 (2024). https://doi.org/10.1007/s12011-023-03756-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-023-03756-3

Keywords

Search

Navigation