Skip to main content
SpringerLink
Log in

Hepatoprotective Effects of Taurine Against Cadmium-Induced Liver Injury in Female Mice

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

Abstract

Cadmium (Cd), a heavy metal contaminant, seriously threatens human and animal health. Taurine (Tau) has been used against hepatotoxicity caused by different environmental toxins. However, it has not been elucidated whether Tau exerts its protective function against Cd-induced hepatotoxicity. The aim of this study was thus to evaluate the ameliorative function of Tau (500 mg/kg body weight intraperitoneally) on Cd-induced (2 mg/kg body weight intraperitoneally) liver toxicity in mice for 14 days. The histopathologic and ultrastructure changes as well as alterations in indexes related to liver function, antioxidant biomarkers, inflammatory, and apoptosis were evaluated. The results showed that Tau alleviated the vacuolar degeneration, nuclear condensation, mitochondria swelling, and cristae lysis of hepatocytes induced by Cd. In addition, Tau treatment significantly reduced the ALT, AST levels in serum, and inflammatory factor TNF-α and IL-1β in liver tissue. Furthermore, Tau treatment decreased the Bax/Bcl-2 ratio and cleaved caspase-3 protein expression levels. Taken together, these observations demonstrate that Tau has an important hepatic protective function against the inflammation and apoptosis induced by Cd.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Data Availability

All data used to support the findings of this study are included within the article.

References

  1. Zhang C, Ge J, Lv M, Zhang Q, Talukder M, Li J (2020) Selenium prevent cadmium-induced hepatotoxicity through modulation of endoplasmic reticulum-resident selenoproteins and attenuation of endoplasmic reticulum stress. Environ Pollut 260:113873

    Article  CAS  Google Scholar 

  2. Ansari M, Ganaie M, Rehman N, Alharthy K, Khan T, Imam F, Ansari M, Al-Harbi N, Jan B, Sheikh I, Hamad A (2019) Protective role of Roflumilast against cadmium-induced cardiotoxicity through inhibition of oxidative stress and NF-κB signaling in rats. Saudi Pharm J 27(5):673–681

    Article  Google Scholar 

  3. Liu X, Tian G, Jiang D, Zhang C, Kong L (2016) Cadmium (Cd) distribution and contamination in Chinese paddy soils on national scale. Environ Sci Pollut Res Int 23(18):17941–17952

    Article  CAS  Google Scholar 

  4. Almeer R, Alarifi S, Alkahtani S, Ibrahim S, Ali D, Moneim A (2018) The potential hepatoprotective effect of royal jelly against cadmium chloride-induced hepatotoxicity in mice is mediated by suppression of oxidative stress and upregulation of Nrf2 expression. Biomed Pharmacother 106:1490–1498

    Article  Google Scholar 

  5. Hyder O, Chung M, Cosgrove D, Herman J, Li Z, Firoozmand A, Gurakar A, Koteish A, Pawlik T (2013) Cadmium exposure and liver disease among US adults. J Gastrointest Surg 17(7):1265–1273

    Article  Google Scholar 

  6. Alshammari G, Al-Qahtani W, AlFaris N, Alzahrani N, Alkhateeb M, Yahya M (2021) Quercetin prevents cadmium chloride-induced hepatic steatosis and fibrosis by downregulating the transcription of miR-21. BioFactors 47(3). https://doi.org/10.1002/biof.1724

  7. He X, Gao J, Hou H, Qi Z, Chen H, Zhang X (2019) Inhibition of Mitochondrial Fatty Acid Oxidation Contributes to Development of Nonalcoholic Fatty Liver Disease Induced by Environmental Cadmium Exposure. Environ Sci Technol 53(23):13992–14000

    Article  CAS  Google Scholar 

  8. Kaur G, Shivanandappa T, Kumar M, Kushwah A (2020) Fumaric acid protect the cadmium-induced hepatotoxicity in rats: owing to its antioxidant, anti-inflammatory action and aid in recast the liver function. Naunyn Schmiedebergs Arch Pharmacol 393(10):1911–1920

    Article  CAS  Google Scholar 

  9. Cao Z, Fang Y, Lu Y, Tan D, Du C, Li Y, Ma Q, Yu J, Chen M, Zhou C, Pei L, Zhang L, Ran H, He M, Yu Z, Zhou Z (2017) Melatonin alleviates cadmium-induced liver injury by inhibiting the TXNIP-NLRP3 inflammasome. J Pineal Res 62(3). https://doi.org/10.1111/jpi.12389

  10. Li X, Li H, Cai D, Li P, Jin J, Jiang X, Li Z, Tian L, Chen G, Sun J, Bai W (2021) Chronic oral exposure to cadmium causes liver inflammation by NLRP3 inflammasome activation in pubertal mice. Food Chem Toxicol 148:111944

    Article  CAS  Google Scholar 

  11. Arab-Nozari M, Mohammadi E, Shokrzadeh M, Ahangar N, Amiri F, Shaki F (2020) Co-exposure to non-toxic levels of cadmium and fluoride induces hepatotoxicity in rats via triggering mitochondrial oxidative damage, apoptosis, and NF-kB pathways. Environ Sci Pollut Res Int 27(19):24048–24058

    Article  CAS  Google Scholar 

  12. Abdel-Daim M, El-Tawil O, Bungau S, Atanasov A (2019) Applications of antioxidants in metabolic disorders and degenerative diseases: mechanistic approach. Oxid Med Cell Longev 2019:4179676

    Article  Google Scholar 

  13. Yeung A, Tzvetkov N, El-Tawil O, Bungǎu S, Abdel-Daim M, Atanasov A (2019) Antioxidants: scientific literature landscape analysis. Oxid Med Cell Longev 2019:8278454

    Article  Google Scholar 

  14. Sun Q, Wang B, Li Y, Sun F, Li P, Xia W, Zhou X, Li Q, Wang X, Chen J, Zeng X, Zhao Z, He H, Liu D, Zhu Z (2016) Taurine supplementation lowers blood pressure and improves vascular function in prehypertension: randomized, double-blind, placebo-controlled study. Hypertension 67(3):541–9

    Article  CAS  Google Scholar 

  15. Marcinkiewicz J, Kontny E (2014) Taurine and inflammatory diseases. Amino acids 46(1):7–20

    Article  CAS  Google Scholar 

  16. Wen C, Li F, Zhang L, Duan Y, Guo Q, Wang W, He S, Li J, Yin Y (2019) Taurine is involved in energy metabolism in muscles, adipose tissue, and the liver. Mol Nutr Food Res 63(2):e1800536

    Article  Google Scholar 

  17. Xu H, Zhang Q, Kim S, Liao Z, Wei Y, Sun B, Jia L, Chi S, Liang M (2020) Takifugu rubripesDietary taurine stimulates the hepatic biosynthesis of both bile acids and cholesterol in the marine teleost, tiger puffer (). Br J Nutr 123(12):1345–1356

    Article  CAS  Google Scholar 

  18. Qvartskhava N, Jin C, Buschmann T, Albrecht U, Bode J, Monhasery N, Oenarto J, Bidmon H, Görg B, Häussinger D (2019) Taurine transporter (TauT) deficiency impairs ammonia detoxification in mouse liver. Proc Natl Acad Sci U S A 116(13):6313–6318

    Article  CAS  Google Scholar 

  19. El Idrissi A (2019) Taurine regulation of neuroendocrine function. Adv Exp Med Biol 1155:977–985

    Article  Google Scholar 

  20. Ahmadian M, Roshan V, Aslani E, Stannard S (2017) Taurine supplementation has anti-atherogenic and anti-inflammatory effects before and after incremental exercise in heart failure. Ther Adv Cardiovasc Dis 11(7):185–194

    Article  CAS  Google Scholar 

  21. Ghosh J, Das J, Manna P, Sil P (2009) Taurine prevents arsenic-induced cardiac oxidative stress and apoptotic damage: role of NF-kappa B, p38 and JNK MAPK pathway. Toxicol Appl Pharmacol 240(1):73–87

    Article  CAS  Google Scholar 

  22. Ashkani-Esfahani S, Zarifi F, Asgari Q, Samadnejad A, Rafiee S, Noorafshan A (2014) Taurine improves the wound healing process in cutaneous leishmaniasis in mice model, based on stereological parameters. Adv Biomed Res 3:204

    Article  Google Scholar 

  23. Terrill J, Pinniger G, Graves J, Grounds M, Arthur P (2016) Increasing taurine intake and taurine synthesis improves skeletal muscle function in the mdx mouse model for Duchenne muscular dystrophy. J Physiol 594(11):3095–3110

    Article  CAS  Google Scholar 

  24. Sirdah M (2015) Protective and therapeutic effectiveness of taurine in diabetes mellitus: a rationale for antioxidant supplementation. Diabetes Metab Syndr 9(1):55–64

    Article  Google Scholar 

  25. Hsiao E, McBride S, Hsien S, Sharon G, Hyde E, McCue T, Codelli J, Chow J, Reisman S, Petrosino J, Patterson P, Mazmanian S (2013) Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155(7):1451–1463

    Article  CAS  Google Scholar 

  26. Abdel-Daim M, Dessouki A, Abdel-Rahman H, Eltaysh R, Alkahtani S (2019) Hepatorenal protective effects of taurine and N-acetylcysteine against fipronil-induced injuries: the antioxidant status and apoptotic markers expression in rats. Sci Total Environ 650:2063–2073

    Article  CAS  Google Scholar 

  27. Han H, Zhang J, Chen Y, Shen M, Yan E, Wei C, Yu C, Zhang L, Wang T (2020) Dietary taurine supplementation attenuates lipopolysaccharide-induced inflammatory responses and oxidative stress of broiler chickens at an early age. J Anim Sci 98(10). https://doi.org/10.1093/jas/skaa311

  28. Sinha M, Manna P, Sil PC (2009) Induction of necrosis in cadmium-induced hepatic oxidative stress and its prevention by the prophylactic properties of taurine. J Trace Elem Med Biol 23(4):300–313

    Article  CAS  Google Scholar 

  29. Liu Y, Li F, Zhang L, Wu J, Wang Y, Yu H (2017) Taurine alleviates lipopolysaccharide-induced liver injury by anti-inflammation and antioxidants in rats. Mol Med Rep 16(5):6512–6517

    Article  CAS  Google Scholar 

  30. Jeong JE, Kim TY, Park HJ, Lee KH, Kim WT (2009) Taurine exerts neuroprotective effects via anti-apoptosis in hypoxic-ischemic brain injury in neonatal rats. Korean J Pediatr 52(12):1337–1347

    Article  Google Scholar 

  31. Zhu X, Ma P, Wu W, Zhou R, Hao Y, Niu Y, Sun T, Li Y, Yu J (2016) Neuroprotective actions of taurine on hypoxic-ischemic brain damage in neonatal rats. Brain Res Bull 124:295–305

    Article  CAS  Google Scholar 

  32. Abdel-Moneim A, Al-Kahtani M, El-Kersh M, Al-Omair M (2015) Free radical-scavenging, anti-inflammatory/anti-fibrotic and hepatoprotective actions of taurine and silymarin against CCl4 induced rat liver damage. PLoS ONE 10(12):e0144509

    Article  Google Scholar 

  33. Wu G, Ren S, Tang R, Xu C, Zhou J, Lin S, Feng Y, Yang Q, Hu J, Yang J (2017) Antidepressant effect of taurine in chronic unpredictable mild stress-induced depressive rats. Sci Rep 7(1):4989

    Article  Google Scholar 

  34. Zheng J, Zhuo L, Ran D, Ma Y, Luo T, Zhao H, Song R, Zou H, Zhu J, Gu J, Bian J, Yuan Y, Liu Z (2020) Cadmium induces apoptosis via generating reactive oxygen species to activate mitochondrial p53 pathway in primary rat osteoblasts. Toxicology 446:152611

    Article  CAS  Google Scholar 

  35. Li S, Yang L, Dong G, Wang X (2017) Taurine protects mouse liver against arsenic-induced apoptosis through JNK pathway. Adv Exp Med Biol :855–862. https://doi.org/10.1007/978-94-024-1079-2_67

  36. Aglan H, Safar M, Ain-Shoka A, Kandil A, Gebremedhn S, Salilew-Wondim D, Schellander K, Tesfaye D (2021) Developmental toxicity of lead in rats after gestational exposure and the protective role of taurine. J Biochem Mol Toxicol 35(8):e22816

    Article  CAS  Google Scholar 

  37. Jagadeesan G, Sankarsami Pillai S (2007) Hepatoprotective effects of taurine against mercury induced toxicity in rats. J Environ Biol 28(4):753–756

    CAS  Google Scholar 

  38. Yuet Ping K, Darah I, Chen Y, Sreeramanan S, Sasidharan S (2013) Acute and subchronic toxicity study of Euphorbia hirta L. methanol extract in rats. BioMed Res Int 2013:182064

    Article  Google Scholar 

  39. Abdel-Wahab W (2014) Thymoquinone attenuates toxicity and oxidative stress induced by bisphenol A in liver of male rats. Pak J Biol Sci 17(11):1152–1160

    Article  CAS  Google Scholar 

  40. Sanjeev S, Bidanchi R, Murthy M, Gurusubramanian G, Roy V (2019) Influence of ferulic acid consumption in ameliorating the cadmium-induced liver and renal oxidative damage in rats. Environ Sci Pollut Res Int 26(20):20631–20653

    Article  CAS  Google Scholar 

  41. Yang Q, Zhu J, Luo X, Li F, Cong L, Wang Y, Sun Y (2019) Melatonin attenuates cadmium-induced ovulatory dysfunction by suppressing endoplasmic reticulum stress and cell apoptosis. Reprod Biol Endocrinol 17(1):61

    Article  Google Scholar 

  42. Nna V, Usman U, Ofutet E, Owu D (2017) Quercetin exerts preventive, ameliorative and prophylactic effects on cadmium chloride-induced oxidative stress in the uterus and ovaries of female Wistar rats. Food Chem Toxicol 102:143–155

    Article  CAS  Google Scholar 

  43. Uzunhisarcikli M, Aslanturk A (2019) Hepatoprotective effects of curcumin and taurine against bisphenol A-induced liver injury in rats. Environ Sci Pollut Res Int 26(36):37242–37253

    Article  CAS  Google Scholar 

  44. Hwang D, Wang L (2001) Effect of taurine on toxicity of cadmium in rats. Toxicology 167(3):173–180

    Article  CAS  Google Scholar 

  45. Gong Z, Wang X, Wang J, Fan R, Wang L (2019) Trehalose prevents cadmium-induced hepatotoxicity by blocking Nrf2 pathway, restoring autophagy and inhibiting apoptosis. J Inorg Biochem 192:62–71

    Article  CAS  Google Scholar 

  46. Dai Z, Cheng J, Bao L, Zhu X, Li H, Chen X, Zhang Y, Zhang J, Chu W, Pan Y, Huang H (2020) Exposure to waterborne cadmium induce oxidative stress, autophagy and mitochondrial dysfunction in the liver of Procypris merus. Ecotoxicol Environ Saf 204:111051

    Article  CAS  Google Scholar 

  47. Ren L, Qi K, Zhang L, Bai Z, Ren C, Xu X, Zhang Z, Li X (2019) Glutathione might attenuate cadmium-induced liver oxidative stress and hepatic stellate cell activation. Biol Trace Elem Res 191(2):443–452

    Article  CAS  Google Scholar 

  48. Amamou F, Nemmiche S, Meziane R, Didi A, Yazit S, Chabane-Sari D (2015) Protective effect of olive oil and colocynth oil against cadmium-induced oxidative stress in the liver of Wistar rats. Food Chem Toxicol 78:177–184

    Article  CAS  Google Scholar 

  49. Zhang Z, Liu D, Yi B, Liao Z, Tang L, Yin D, He M (2014) Taurine supplementation reduces oxidative stress and protects the liver in an iron-overload murine model. Mol Med Rep 10(5):2255–2262

    Article  CAS  Google Scholar 

  50. Parildar-Karpuzoğlu H, Mehmetçik G, Ozdemirler-Erata G, Doğru-Abbasoğlu S, Koçak-Toker N, Uysal M (2008) Effect of taurine treatment on pro-oxidant-antioxidant balance in livers and brains of old rats. Pharmacol Rep 60(5):673–678

    Google Scholar 

  51. Liu L, Tao R, Huang J, He X, Qu L, Jin Y, Zhang S, Fu Z (2015) Hepatic oxidative stress and inflammatory responses with cadmium exposure in male mice. Environ Toxicol Pharmacol 39(1):229–236

    Article  CAS  Google Scholar 

  52. Eşrefoglu M, Gül M, Dogru M, Dogru A, Yürekli M (2007) Adrenomedullin fails to reduce cadmium-induced oxidative damage in rat liver. Exp Toxicol Pathol 58(5):367–374

    Article  Google Scholar 

  53. Shimada H, Hashiguchi T, Yasutake A, Waalkes M, Imamura Y (2012) Sexual dimorphism of cadmium-induced toxicity in rats: involvement of sex hormones. Arch Toxicol 86(9):1475–1480

    Article  CAS  Google Scholar 

  54. Lee J, Lim K (2011) Preventive effect of phytoglycoprotein (27 kDa) on inflammatory factors at liver injury in cadmium chloride-exposed ICR mice. J Cell Biochem 112(2):694–703

    Article  CAS  Google Scholar 

  55. Barua M, Liu Y, Quinn M (2001) Taurine chloramine inhibits inducible nitric oxide synthase and TNF-alpha gene expression in activated alveolar macrophages: decreased NF-kappaB activation and IkappaB kinase activity. J immunol 167(4):2275–81

    Article  CAS  Google Scholar 

  56. Jong C, Azuma J, Schaffer S (2012) Mechanism underlying the antioxidant activity of taurine: prevention of mitochondrial oxidant production. Amino Acids 42(6):2223–2232

    Article  CAS  Google Scholar 

  57. El-Maraghi E, Abdel-Fattah K, Soliman S, El-Sayed W (2020) Taurine abates the liver damage induced by γ-irradiation in rats through anti-inflammatory and anti-apoptotic pathways. Int J Radiat Biol 96(12):1550–1559

    Article  CAS  Google Scholar 

  58. Wu G, Yang J, Lv H, Jing W, Zhou J, Feng Y, Lin S, Yang Q, Hu J (2018) Taurine prevents ethanol-induced apoptosis mediated by mitochondrial or death receptor pathways in liver cells. Amino Acids 50(7):863–875

    Article  CAS  Google Scholar 

Download references

Funding

This work is supported by the Natural Science Foundation of China (31772692) and the Project of the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

Author information

Author notes

  1. Jiaming Zheng and Guobin Qiu contributed equally to this work.

Authors and Affiliations

  1. College of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, 225009, People’s Republic of China

    Jiaming Zheng, Guobin Qiu, Yewen Zhou, Kezhe Ma & Sheng Cui

  2. Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, Jiangsu, 225009, People’s Republic of China

    Jiaming Zheng, Guobin Qiu, Yewen Zhou, Kezhe Ma & Sheng Cui

  3. Joint International Research Laboratory of Agriculture and Agri-Product Safety of the Ministry of Education of China, Yangzhou University, Yangzhou, China

    Jiaming Zheng, Guobin Qiu, Yewen Zhou, Kezhe Ma & Sheng Cui

Authors
  1. Jiaming Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guobin Qiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yewen Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kezhe Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sheng Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Sheng Cui contributed to the conception of the study. Jiaming Zheng and Guobin Qiu performed experiment, collected and analyzed data, and wrote the paper. Yewen Zhou and Kezhe Ma contributed significantly to analysis and manuscript preparation. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Sheng Cui.

Ethics declarations

Ethics Approval

All procedures were approved by the Animal Care and Use Committee at Yangzhou University (approval ID: SYXK (Su) 2017–0044).

Consent to Participate

Not applicable.

Consent for Publication

The authors confirm that the work described has not been published before.

Competing Interests

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.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 174 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zheng, J., Qiu, G., Zhou, Y. et al. Hepatoprotective Effects of Taurine Against Cadmium-Induced Liver Injury in Female Mice. Biol Trace Elem Res 201, 1368–1376 (2023). https://doi.org/10.1007/s12011-022-03252-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-022-03252-0

Keywords

Search

Navigation