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Lactobacillus plantarum CCFM8661 Alleviates Lead Toxicity in Mice

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Abstract

Lead causes a broad range of adverse effects in humans and animals. The objective was to evaluate the potency of lactobacilli to bind lead in vitro and the protective effects of a selected Lactobacillus plantarum CCFM8661 against lead-induced toxicity in mice. Nine strains of bacteria were used to investigate their binding abilities of lead in vitro, and L. plantarum CCFM8661 was selected for animal experiments because of its excellent lead binding capacity. Both living and dead L. plantarum CCFM8661 were used to treat 90 male Kunming mice during or after the exposure to 1 g/L lead acetate in drinking water. The results showed oral administration of both living and dead L. plantarum CCFM8661 offered a significant protective effect against lead toxicity by recovering blood δ-aminolevulinic acid dehydratase activity, decreasing the lead levels in blood and tissues, and preventing alterations in the levels of glutathione, glutathione peroxidase, malondialdehyde, superoxide dismutase, and reactive oxygen species caused by lead exposure. Moreover, L. plantarum CCFM8661 was more effective when administered consistently during the entire lead exposure, not after the exposure. Our results suggest that L. plantarum CCFM8661 has the potency to provide a dietary strategy against lead toxicity.

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References

  1. Mielke HW (2002) Research ethics in pediatric environmental health: lessons from lead. Neurotoxicol Teratol 24(4):467–469

    Article  PubMed  CAS  Google Scholar 

  2. Fewtrell L, Pruss-ustan A, Landrigan P, Ayuso-Mateos J (2004) Estimating the global burden of disease of mild mental retardation and cardiovascular diseases from environmental lead exposure* 1. Environ Res 94(2):120–133

    Article  PubMed  CAS  Google Scholar 

  3. Solon O, Riddell TJ, Quimbo SA, Butrick E, Aylward GP, Lou Bacate M, Peabody JW (2008) Associations between cognitive function, blood lead concentration, and nutrition among children in the central Philippines. J Pediatr 152(2):237–243, e231

    Article  PubMed  CAS  Google Scholar 

  4. Ahamed M, Siddiqui M (2007) Environmental lead toxicity and nutritional factors. Clin Nutr 26(4):400–408

    Article  PubMed  CAS  Google Scholar 

  5. Farmand F, Ehdaie A, Roberts CK, Sindhu RK (2005) Lead-induced dysregulation of superoxide dismutases, catalase, glutathione peroxidase, and guanylate cyclase. Environ Res 98(1):33–39

    Article  PubMed  CAS  Google Scholar 

  6. Fracasso ME, Perbellini L, Sold S, Talamini G, Franceschetti P (2002) Lead induced DNA strand breaks in lymphocytes of exposed workers: role of reactive oxygen species and protein kinase C* 1. Mutat Res-Gen Tox En 515(1–2):159–169

    Article  CAS  Google Scholar 

  7. Gurer H, Ercal N (2000) Can antioxidants be beneficial in the treatment of lead poisoning? Free Radical Bio Med 29(10):927–945

    Article  CAS  Google Scholar 

  8. Aposhian HV, Maiorino RM, Gonzalez-Ramirez D, Zuniga-Charles M, Xu Z, Hurlbut KM, Junco-Munoz P, Dart RC, Aposhian M (1995) Mobilization of heavy metals by newer, therapeutically useful chelating agents. Toxicology 97(1–3):23–38

    Article  PubMed  Google Scholar 

  9. Chisolm JJ Jr (1990) Evaluation of the potential role of chelation therapy in treatment of low to moderate lead exposures. Environ Health Persp 89:67–74

    Article  Google Scholar 

  10. Pappas J, Ahlquist J, Allen E, Banner W (1995) Oral dimercaptosuccinic acid and ongoing exposure to lead: effects on heme synthesis and lead distribution in a rat model. Toxicol Appl Pharm 133(1):121–129

    Article  CAS  Google Scholar 

  11. Porru S, Alessio L (1996) The use of chelating agents in occupational lead poisoning. Occup Med 46(1):41–48

    Article  CAS  Google Scholar 

  12. Jorgensen F (1993) Succimer: the first approved oral lead chelator. Am Fam Physician 48(8):1496–1502

    PubMed  CAS  Google Scholar 

  13. Rolfe RD (2000) The role of probiotic cultures in the control of gastrointestinal health. J Nutr 130(2S Suppl):396S–402S

    PubMed  CAS  Google Scholar 

  14. Gill H, Guarner F (2004) Probiotics and human health: a clinical perspective. Postgrad Med J 80(947):516–526

    Article  PubMed  CAS  Google Scholar 

  15. Lyte M (2011) Probiotics function mechanistically as delivery vehicles for neuroactive compounds: microbial endocrinology in the design and use of probiotics. BioEssays 33(8):574–581

    Article  PubMed  CAS  Google Scholar 

  16. Halttunen T, Collado MC, El-Nezami H, Meriluoto J, Salminen S (2007) Combining strains of lactic acid bacteria may reduce their toxin and heavy metal removal efficiency from aqueous solution. Lett Appl Microbiol 46(2):160–165. doi:10.1111/j.1472-765X.2007.02276.x

    Article  PubMed  Google Scholar 

  17. Romera E, González F, Ballester A, Blázquez ML, Muñoz JA (2007) Comparative study of biosorption of heavy metals using different types of algae. Bioresource Technol 98(17):3344–3353. doi:10.1016/j.biortech.2006.09.026

    Article  CAS  Google Scholar 

  18. Fan T, Liu Y, Feng B, Zeng G, Yang C, Zhou M, Zhou H, Tan Z, Wang X (2008) Biosorption of cadmium(II), zinc(II) and lead(II) by Penicillium simplicissimum: isotherms, kinetics and thermodynamics. J Hazard Mater 160(2–3):655–661. doi:10.1016/j.jhazmat.2008.03.038

    Article  PubMed  CAS  Google Scholar 

  19. Mrvcic J, Stanzer D, Bacun-Druzina V, Stehlik-Tomas V (2009) Copper binding by lactic acid bacteria (LAB). Biosci Microflora 28(1):1–6

    CAS  Google Scholar 

  20. Forsyth CB, Farhadi A, Jakate SM, Tang Y, Shaikh M, Keshavarzian A (2009) Lactobacillus GG treatment ameliorates alcohol-induced intestinal oxidative stress, gut leakiness, and liver injury in a rat model of alcoholic steatohepatitis. Alcohol 43(2):163–172. doi:10.1016/j.alcohol.2008.12.009

    Article  PubMed  CAS  Google Scholar 

  21. Xing H, Li L, Xu K, Shen T, Chen Y, Sheng J, Chen Y, Fu S, Chen C, Wang J, Yan D, Dai F, Zheng S (2006) Protective role of supplement with foreign Bifidobacterium and Lactobacillus in experimental hepatic ischemia-reperfusion injury. J Gastroen Hepatol 21(4):647–656

    Article  Google Scholar 

  22. Kullisaar T, Songisepp E, Mikelsaar M, Zilmer K, Vihalemm T, Zilmer M (2007) Antioxidative probiotic fermented goats’ milk decreases oxidative stress-mediated atherogenicity in human subjects. Brit J Nutr 90(02):449–456. doi:10.1079/bjn2003896

    Article  Google Scholar 

  23. Aksu Z, Donmez G (2001) Comparison of copper(II) biosorptive properties of live and treated Candida sp. J Environ Sci Heal A 36(3):367–381

    CAS  Google Scholar 

  24. Flora S, Bhattacharya R, Vijayaraghavan R (1995) Combined therapeutic potential of meso-2, 3-dimercaptosuccinic acid and calcium disodium edetate on the mobilization and distribution of lead in experimental lead intoxication in rats. Toxicol Sci 25(2):233–240

    Article  CAS  Google Scholar 

  25. Flora SJS, Pande M, Mehta A (2003) Beneficial effect of combined administration of some naturally occurring antioxidants (vitamins) and thiol chelators in the treatment of chronic lead intoxication. Chem-Biol Interact 145(3):267–280. doi:10.1016/s0009-2797(03)00025-5

    Article  PubMed  CAS  Google Scholar 

  26. Tangpong J, Satarug S (2010) Alleviation of lead poisoning in the brain with aqueous leaf extract of the Thunbergia laurifolia (Linn.). Toxicol Lett 198(1):83–88. doi:10.1016/j.toxlet.2010.04.031

    Article  PubMed  CAS  Google Scholar 

  27. Penugonda S, Ercal N (2011) Comparative evaluation of N-acetylcysteine (NAC) and N-acetylcysteine amide (NACA) on glutamate and lead-induced toxicity in CD-1 mice. Toxicol Lett 201(1):1–7. doi:10.1016/j.toxlet.2010.11.013

    Article  PubMed  CAS  Google Scholar 

  28. Berlin A, Schaller K (1974) European standardized method for the determination of delta-aminolevulinic acid dehydratase activity in blood. Z Klin Chem Klin Biochem 12(8):389–390

    PubMed  CAS  Google Scholar 

  29. Esfandiari N, Sharma RK, Saleh RA, Thomas AJ Jr, Agarwal A (2003) Utility of the nitroblue tetrazolium reduction test for assessment of reactive oxygen species production by seminal leukocytes and spermatozoa. J Androl 24(6):862–870

    PubMed  CAS  Google Scholar 

  30. Cholak J, Yeager DW, Henderson EW (1971) Determination of lead in biological and related material by atomic absorption spectrophotometry. Environ Sci Technol 5(10):1020–1022

    Article  CAS  Google Scholar 

  31. Schut S, Zauner S, Hampel G, König H, Claus H (2011) Biosorption of copper by wine-relevant lactobacilli. Int J Food Microbiol 145(1):126–131. doi:10.1016/j.ijfoodmicro.2010.11.039

    Article  PubMed  CAS  Google Scholar 

  32. Halttunen T, Salminen S, Tahvonen R (2007) Rapid removal of lead and cadmium from water by specific lactic acid bacteria. Int J Food Microbiol 114(1):30–35. doi:10.1016/j.ijfoodmicro.2006.10.040

    Article  PubMed  CAS  Google Scholar 

  33. Ibrahim F, Halttunen T, Tahvonen R, Salminen S (2006) Probiotic bacteria as potential detoxification tools: assessing their heavy metal binding isotherms. Can J Microbiol 52(9):877–885. doi:10.1139/w06-043

    Article  PubMed  CAS  Google Scholar 

  34. Dursun AY, Uslu G, Cuci Y, Aksu Z (2003) Bioaccumulation of copper(II), lead(II) and chromium(VI) by growing Aspergillus niger. Process Biochem 38(12):1647–1651. doi:10.1016/s0032-9592(02)00075-4

    Article  CAS  Google Scholar 

  35. Bueno B, Torem M, Molina F, Demesquita L (2008) Biosorption of lead(II), chromium(III) and copper(II) by R. opacus: equilibrium and kinetic studies. Miner Eng 21(1):65–75. doi:10.1016/j.mineng.2007.08.013

    Article  CAS  Google Scholar 

  36. Delcour J, Ferain T, Deghorain M, Palumbo E, Hols P (1999) The biosynthesis and functionality of the cell-wall of lactic acid bacteria. Anton Leeuw Int J G 76(1):159–184

    Article  CAS  Google Scholar 

  37. Teemu H, Seppo S, Jussi M, Raija T, Kalle L (2008) Reversible surface binding of cadmium and lead by lactic acid and bifidobacteria. Int J Food Microbiol 125(2):170–175. doi:10.1016/j.ijfoodmicro.2008.03.041

    Article  PubMed  CAS  Google Scholar 

  38. Gabr RM, Hassan SHA, Shoreit AAM (2008) Biosorption of lead and nickel by living and non-living cells of Pseudomonas aeruginosa ASU 6a. Int Biodeter Biodegr 62(2):195–203. doi:10.1016/j.ibiod.2008.01.008

    Article  CAS  Google Scholar 

  39. Özer A, Özer D (2003) Comparative study of the biosorption of Pb (II), Ni (II) and Cr (VI) ions onto S. cerevisiae: determination of biosorption heats. J Hazard Mater 100(1):219–229

    Article  PubMed  Google Scholar 

  40. Srinath T, Verma T, Ramteke P, Garg S (2002) Chromium (VI) biosorption and bioaccumulation by chromate resistant bacteria. Chemosphere 48(4):427–435

    Article  PubMed  CAS  Google Scholar 

  41. DeSilva P (1981) Determination of lead in plasma and studies on its relationship to lead in erythrocytes. Brit J Ind Med 38(3):209–217

    CAS  Google Scholar 

  42. Leggett RW (1993) An age-specific kinetic model of lead metabolism in humans. Environ Health Persp 101(7):598–616

    Article  CAS  Google Scholar 

  43. Monteiro HP, Bechara EJH, Abdalla DSP (1991) Free radicals involvement in neurological porphyrias and lead poisoning. Mol Cell Biochem 103(1):73–83

    Article  PubMed  CAS  Google Scholar 

  44. Hermes-Lima M, Valle VGR, Vercesi AE, Bechara EJH (1991) Damage to rat liver mitochondria promoted by [delta]-aminolevulinic acid-generated reactive oxygen species: connections with acute intermittent porphyria and lead-poisoning. BBA-Bioenergetics 1056(1):57–63

    Article  PubMed  CAS  Google Scholar 

  45. Heales R, Davies S, Bates T, Clark J (1995) Depletion of brain glutathione is accompanied by impaired micochondrial function and decreased N-acetyl aspartate concentration. Neurochem Res 20(1):31–38

    Article  PubMed  CAS  Google Scholar 

  46. Pereira CF, Oliveira CR (2000) Oxidative glutamate toxicity involves mitochondrial dysfunction and perturbation of intracellular Ca2+ homeostasis. Neurosci Res 37(3):227–236

    Article  PubMed  CAS  Google Scholar 

  47. Chen L, Pan DD, Zhou J, Jiang YZ (2005) Protective effect of selenium-enriched lactobacillus on CCl4-induced liver injury in mice and its possible mechanisms. World J Gastroentero 11(37):5795–5800

    CAS  Google Scholar 

  48. Zhang Y, Du R, Wang L, Zhang H (2010) The antioxidative effects of probiotic Lactobacillus casei Zhang on the hyperlipidemic rats. Eur Food Res Technol 231(1):151–158

    Article  CAS  Google Scholar 

  49. Güven A, Gülmez M (2003) The effect of kefir on the activities of GSH–Px, GST, CAT, GSH and LPO levels in carbon tetrachloride-induced mice tissues. J Vet Intern Med 50(8):412–416

    Article  Google Scholar 

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Acknowledgments

This work was supported by the National Science Fund for Distinguished Young Scholars (no. 31125021), the National High Technology Research and Development Program of China (no. 2011AA100901,2011AA100902), National Natural Science Foundation of China (no. 20836003), the National Basic Research Program of China 973 Program (no. 2012CB720802), the National Science and Technology Pillar Program (no. 2010C0070311), the 111 project B07029, Fundamental Research Funds for the Central Universities (JUSRP111A31 and JUSRP31103), and SKLF-MB-200802.

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Authors and Affiliations

  1. State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, 214122, People’s Republic of China

    Fengwei Tian & Wei Chen

  2. School of Food Science and Technology, Jiangnan University, Wuxi, 214122, People’s Republic of China

    Qixiao Zhai, Jianxin Zhao, Xiaoming Liu, Gang Wang & Hao Zhang

  3. Key Laboratory of Dairy Biotechnology and Engineering, Ministry of Education, Inner Mongolia Agricultural University, Hohhot, Inner Mongolia, 010018, China

    Heping Zhang

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  1. Fengwei Tian
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Correspondence to Wei Chen.

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Fengwei Tian and Qixiao Zhai made equal contributions to this work.

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Tian, F., Zhai, Q., Zhao, J. et al. Lactobacillus plantarum CCFM8661 Alleviates Lead Toxicity in Mice. Biol Trace Elem Res 150, 264–271 (2012). https://doi.org/10.1007/s12011-012-9462-1

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  • DOI: https://doi.org/10.1007/s12011-012-9462-1

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