Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Potential Protective Effect of Selenium-Enriched Lactobacillus plantarum on Cadmium-Induced Liver Injury in Mice

  • Yanyan Song (College of Biochemical Engineering, Beijing Union University) ;
  • Jing Zhang (College of Biochemical Engineering, Beijing Union University) ;
  • Yidan Li (College of Biochemical Engineering, Beijing Union University) ;
  • Yuxuan Wang (College of Biochemical Engineering, Beijing Union University) ;
  • Yingxin Wan (College of Biochemical Engineering, Beijing Union University)
  • Received : 2024.01.02
  • Accepted : 2024.04.05
  • Published : 2024.06.28
Download PDF
⟨ Previous Next ⟩

Abstract

Cadmium (Cd) is a prevalent environmental contaminant that poses a potential hazard to the health of both humans and animals. In this study, biosynthesized selenium-enriched Lactobacillus plantarum and selenium nanoparticles (SeNPs) were developed and evaluated for their protective effects against Cd-induced hepatic injury in mice through oral administration for 4 weeks. Cadmium exposure resulted in severe impairment of liver function, as evidenced by increased levels of serum markers of liver injury and, oxidative stress and significant damage to liver tissue, and a notable decrease in the diversity of the intestinal microbiota. Oral administration of Se-enriched L. plantarum (LS) reduced cadmium accumulation in the liver by 49.5% and, restored other cadmium-induced damage markers to normal levels. A comparison of the effects with those of L. plantarum (L) and SeNPs isolated from LS revealed that LS could more effectively alleviate hepatic oxidative stress and reduce the intrahepatic inflammatory responses of the liver, further protecting against cadmium-induced liver injury. These findings suggest that the development of LS may be effective at protecting the liver and intestinal tract from cadmium-induced damage.

Keywords

Acknowledgement

This work was supported by the Science and Technology Project of Beijing Union University (ZK30202302) and the Education and Teaching Research and Reform Project of Beijing Union University (JJ2022Y020).

References

  1. Zan Z, Chen K, Wang H, Han Z, Sun J. 2023. Effects of a multistrain probiotic on the growth, immune function and intestinal microbiota of the tongue sole. Cynoglossus semilaevis. Aquaculture 575: 739813. 
  2. Kim HS, Kim YJ, Seo YR. 2015. An overview of carcinogenic heavy metal: molecular toxicity mechanism and prevention. J. Cancer Prev. 20: 232. 
  3. Duan H, Yu L, Tian F, Zhai Q, Fan L, Chen W. 2020. Gut microbiota: a target for heavy metal toxicity and a probiotic protective strategy. Sci. Total. Environ. 742: 140429. 
  4. Kakade A, Sharma M, Salama ES, Zhang P, Zhang L, Xing X, et al. 2023. Heavy Metals (HMs) pollution in the aquatic environment: role of probiotics and gut microbiota in HMs remediation. Environ. Res. 223: 115186. 
  5. Jafarpour D, Shekarforoush SS, Ghaisari HR, Nazifi S, Sajedianfard J, Eskandari MH. 2017. Protective effects of synbiotic diets of Bacillus coagulans, Lactobacillus plantarum and inulin against acute cadmium toxicity in rats. BMC Complement. Altern. Med. 17: 291. 
  6. Fan H, Shen Y, Ren Y, Mou Q, Lin T, Zhu L, et al. 2021. Combined intake of blueberry juice and probiotics ameliorate mitochondrial dysfunction by activating SIRT1 in alcoholic fatty liver disease. Nutr. Metab. (Lond) 18: 50. 
  7. Jantararussamee C, Rodniem S, Taweechotipatr M, Showpittapornchai U, Pradidarcheep W. 2021. Hepatoprotective effect of probiotic lactic acid bacteria on thioacetamide-induced liver fibrosis in rats. Probiotics Antimicrob. Proteins 13: 40-50. 
  8. Chen S, Jiang PP, Yu D, Liao GC, Wu SL, Fang AP, et al. 2021. Effects of probiotic supplementation on serum trimethylamine-N-oxide level and gut microbiota composition in young males: a double-blinded randomized controlled trial. Eur. J. Nutr. 60: 747-758. 
  9. Adam-Dima EI, Balas M, Anastasescu M, Purdel C, Margina D. 2024. Synthesis of homogeneous spherical selenium nanoparticles through a chemical method for cancer therapy applications. Toxicol. In Vitro 95: 105765. 
  10. Zhao B, Zhao J, Zhou S, Wu X, Xu X, Yang R, et al. 2023. Selenium and toxic metals in human hair of the Dashan Region, China: concentrations, sources, and antagonism effect. Ecotoxicol. Environ. Saf. 250: 114479. 
  11. Eddie-Amadi BF, Ezejiofor AN, Orish CN. 2022. Orisakwe OE. Zinc and selenium mitigated heavy metals mixture (Pb, Al, Hg and Mn) mediated hepatic-nephropathy via modulation of oxido-inflammatory status and NF-kB signaling in female albino rats. Toxicology 481: 153350. 
  12. Shen Y, Huang H, Wang Y, Yang R, Ke X. 2022. Antioxidant effects of Se-glutathione peroxidase in alcoholic liver disease. J. Trace Elem. Med. Biol. 74: 127048. 
  13. Lu H, Xia Q, Wang Z, Guan N, Zhou Q. 2021. Study on selenium antagonizing cadmium induced liver oxidative damage in mice. Feed Review 3: 20-23. 
  14. Wang R, Sang P, Guo Y, Jin P, Cheng Y, Yu H, et al. 2023. Cadmium in food: source, distribution and removal. Food Chem. 405: 134666. 
  15. Young JL, Cai L. 2020. Implications for prenatal cadmium exposure and adverse health outcomes in adulthood. Toxicol. Appl. Pharmacol. 403: 115161. 
  16. Zhu J, Yu L, Shen X, Tian F, Zhao J, Zhang H, et al. 2021. Protective effects of Lactobacillus plantarum CCFM8610 against acute toxicity caused by different food-derived forms of cadmium in mice. Int. J. Mol. Sci. 22: 11045. 
  17. Groten JP, Sinkeldam EJ, Luten JB, van Bladeren PJ. 1991. Cadmium accumulation and metallothionein concentrations after 4-week dietary exposure to cadmium chloride or cadmium-metallothionein in rats. Toxicol. Appl. Pharmacol. 111: 504-513. 
  18. Tinkov AA, Gritsenko VA, Skalnaya MG, Cherkasov SV, Aaseth J, Skalny AV. 2018. Gut as a target for cadmium toxicity. Environ. Pollut. 235: 429-434. 
  19. Elafify M, EL-Toukhy M, Sallam KI, Sadoma NM, Abd-Elghany SM, Abdelkhalek A, et al. 2023. Heavy metal residues in milk and some dairy products with insight into their health risk assessment and the role of Lactobacillus rhamnosus in reducing the lead and cadmium load in cheese. Food Chem. Adv. 2: 100261. 
  20. Shakibaie M, Mohammadi-Khorsand T, Adeli-Sardou M, Jafari M, Amirpour-Rostami S, Ameri A, et al. 2017. Probiotic and antioxidant properties of selenium-enriched Lactobacillus brevis LSe isolated from an Iranian traditional dairy product. J. Trace Elem. Med. Biol. 40: 1-9. 
  21. Liu J, Shi L, Tuo X, Ma X, Hou X, Jiang S, et al. 2022. Preparation, characteristic and anti-inflammatory effect of selenium nanoparticle-enriched probiotic strain Enterococcus durans A8-1. J. Trace Elem. Med. Biol. 74: 127056. 
  22. Shang X, Sun Q, Yin Y, Zhang Y, Zhang P, Mao Q, et al. 2021. Reducing mercury accumulation in common carp using selenium-enriched Bacillus subtilis. Aquac. Rep. 19: 100609. 
  23. Jin H, Riaz Rajoka MS, Xu X, Liao N, Pang B, Yan L, et al. 2022. Potentials of orally supplemented selenium-enriched Lacticaseibacillus rhamnosus to mitigate the lead induced liver and intestinal tract injury. Environ. Pollut. 302: 119062. 
  24. Xu C, Qiao L, Guo Y, Ma L, Cheng Y. 2018. Preparation, characteristics and antioxidant activity of polysaccharides and proteins-capped selenium nanoparticles synthesized by Lactobacillus casei ATCC 393. Carbohydr. Polym. 195: 576-585. 
  25. Zhang G, Yao X, Wang C, Wang D, Wei G. 2019. Transcriptome analysis reveals the mechanism underlying improved glutathione biosynthesis and secretion in Candida utilis during selenium enrichment. J. Biotechnol. 304: 89-96. 
  26. Shi XD, Tian YQ, Wu JL, Wang SY. 2021. Synthesis, characterization, and biological activity of selenium nanoparticles conjugated with polysaccharides. Crit. Rev. Food Sci. Nutr. 61: 2225-2236. 
  27. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. 2007. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39: 44-84. 
  28. Yohannes YB, Nakayama SMM, Yabe J, Toyomaki H, Kataba A, Nakata H, et al. 2022. Glutathione S-transferase gene polymorphisms in association with susceptibility to lead toxicity in lead- and cadmium-exposed children near an abandoned lead-zinc mining area in Kabwe, Zambia. Environ. Sci. Pollut. Res. Int. 29: 6622-6632. 
  29. Moya A, Ferrer M. 2016. Functional redundancy-induced stability of gut microbiota subjected to disturbance. Trends Microbiol. 24: 402-413. 
  30. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444: 1027-31. 
  31. Bunker JJ, Flynn TM, Koval JC, Shaw DG, Meisel M, McDonald BD, et al. 2015. Innate and Adaptive humoral responses coat distinct commensal bacteria with immunoglobulin A. Immunity 43: 541-553. 
  32. Wang P, Gao J, Ke W, Wang J, Li D, Liu R, et al. 2020. Resveratrol reduces obesity in high-fat diet-fed mice via modulating the composition and metabolic function of the gut microbiota. Free Radic Biol. Med. 156: 83-98. 
  33. Seo B, Jeon K, Moon S, Lee K, Kim WK, Jeong H, et al. 2020. Roseburia spp. Abundance associates with alcohol consumption in humans and its administration ameliorates alcoholic fatty liver in mice. Cell Host Microbe 27: 25-40.e6. 
  34. Martinez de Victoria Carazo J, Vinuesa Garcia D, Serrano-Conde Sanchez E, Peregrina Rivas JA, Ruiz Rodriguez AJ, Hernandez Quero J. 2023. Ruminococcus gnavus bacteremia: literature review and a case report associated with acute flare of ulcerative colitis in an immunocompromised patient. Anaerobe 82:102762. 
  35. Wu X, Chen S, Yan Q, Yu F, Shao H, Zheng X, et al. 2023. Gpr35 shapes gut microbial ecology to modulate hepatic steatosis. Pharmacol. Res. 189:106690. 
  36. Dong J, Liang Q, Niu Y, Jiang S, Zhou L, Wang J, et al. 2020. Effects of Nigella sativa seed polysaccharides on type 2 diabetic mice and gut microbiota. Int. J. Biol. Macromol. 159: 725-738. 
  37. Zhao Liu, Sharmeen Fayyaz, Di Zhao, Ziyang Yi, Jian-hua Huang, Rong-rong Zhou. 2023. Polygonatum sibiricum polysaccharides improve cognitive function in D-galactose-induced aging mice by regulating the microbiota-gut-brain axis. J. Funct. Foods 103: 105476. 
  38. Yang JL, Chen S, Xi JF, Lin XY, Xue RY, Ma LQ, et al. 2024. Sex-dependent effects of rice cadmium exposure on body weight, gut microflora, and kidney metabolomics based on a mouse model. Sci. Total. Environ. 908: 168498. 
  39. Zhang C, Huang Y, Talukder M, Ge J, Lv MW, Bi SS, et al. 2020. Selenium sources differ in their potential to alleviate the cadmium-induced testicular dysfunction. Environ. Pollut. 267: 115610. 
  40. Ge J, Liu LL, Cui ZG, Talukder M, Lv MW, Li JY, et al. 2021. Comparative study on protective effect of different selenium sources against cadmium-induced nephrotoxicity via regulating the transcriptions of selenoproteome. Ecotoxicol. Environ. Saf. 215: 112135. 
  41. Go YM, Sutliff RL, Chandler JD, Khalidur R, Kang BY, Anania FA, et al. 2015. Low-dose cadmium causes metabolic and genetic dysregulation associated with fatty liver disease in mice. Toxicol. Sci. 147: 524-534. 
  42. Dan Zhao, Fei Gao, Hui Zhu, Zhixiang Qian, Wenwei Mao, Yu Yin, et al. 2020. Selenium-enriched Bifidobacterium longum DD98 relieves metabolic alterations and liver injuries associated with obesity in high-fat diet-fed mice. J. Funct. Foods 72: 104051. 
  43. Li X, Li H, Cai D, Li P, Jin J, Jiang X, et al. 2021. Chronic oral exposure to cadmium causes liver inflammation by NLRP3 inflammasome activation in pubertal mice. Food Chem. Toxicol. 148: 111944. 
  44. Salama SA, Arab HH, Hassan MH, Al Robaian MM, Maghrabi IA. 2019. Cadmium-induced hepatocellular injury: modulatory effects of γ-glutamyl cysteine on the biomarkers of inflammation, DNA damage, and apoptotic cell death. J. Trace Elem. Med. Biol. 52: 74-82. 
  45. Liu J, Wu D, Leng Y, Li Y, Li N. 2023. Dietary supplementation with selenium polysaccharide from selenium-enriched Phellinus linteus improves antioxidant capacity, immunity and production performance of laying hens. J. Trace Elem. Med. Biol. 77: 127140. 
  46. Li B, Liu Y, Li W, Tian Y, Xu D, Cao N. 2018. Effect of Selenium on ion profiles and antioxidant defense in mice livers. Biol. Trace Elem. Res. 184: 127-135. 
  47. Wu H, Zheng L, Tan M, Li Y, Xu J, Yan S, et al. 2022. Cd exposure-triggered susceptibility to Bacillus thuringiensis in Lymantria dispar involves in gut microbiota dysbiosis and hemolymph metabolic disorder. Ecotoxicol. Environ. Saf. 241: 113763. 
  48. Zhai Q, Tian F, Zhao J, Zhang H, Narbad A, Chen W. 2016. Oral Administration of probiotics inhibits absorption of the heavy metal cadmium by protecting the intestinal barrier. Appl. Environ. Microbiol. 82: 4429-4440. 
  49. Bi SS, Talukder M, Jin HT, Lv MW, Ge J, Zhang C, et al. 2022. Nano-selenium alleviates cadmium-induced cerebellar injury by activating metal regulatory transcription factor 1 mediated metal response. Anim. Nutr. 11: 402-412. 
  50. Li Wu, Wenlong Li, Guimei Chen, Ziyi Yang, Xucong Lv, Lizhong Zheng, et al. 2022. Ameliorative effects of monascin from red mold rice on alcoholic liver injury and intestinal microbiota dysbiosis in mice. Food Biosci. 50: 102079.