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In Vitro Evaluation of the Protective Role of Lactobacillus StrainsAgainst Inorganic Arsenic Toxicity

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Abstract

Inorganic arsenic [iAs, As(III) + As(V)] is considered a human carcinogen. Recent studies show that it has also toxic effects on the intestinal epithelium which might partly explain its systemic toxicity. The aim of this study is to evaluate the protective role of lactic acid bacteria (LAB) against the toxic effects of iAs on the intestinal epithelium. For this purpose, the human colonic cells Caco-2 were exposed to As(III) in the presence of various LAB strains or their conditioned medium. Results showed that some strains and their conditioned media partially revert the oxidative stress, the production of pro-inflammatory cytokines, the alterations of the distribution of tight junction proteins, and the cell permeability increases caused by As(III). These results show that both soluble factors secreted or resulting from LAB metabolism and cell-cell interactions are possibly involved in the beneficial effects. Therefore, some LAB strains have potential as protective agents against iAs intestinal barrier disruption.

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References

  1. Almela C, Clemente MJ, Velez D, Montoro R (2006) Total arsenic, inorganic arsenic, lead and cadmium contents in edible seaweed sold in Spain. Food Chem Toxicol 44(11):1901–1908. https://doi.org/10.1016/j.fct.2006.06.011

    Article  CAS  Google Scholar 

  2. Bundschuh J, Litter MI, Parvez F, Román-Ross G, Nicolli HB, Jean J-S, Liu C-W, López D, Armienta MA, Guilherme LR (2012) One century of arsenic exposure in Latin America: a review of history and occurrence from 14 countries. Sci Total Environ 429:2–35. https://doi.org/10.1016/j.scitotenv.2011.06.024

    Article  CAS  Google Scholar 

  3. Yunus FM, Khan S, Chowdhury P, Milton AH, Hussain S, Rahman M (2016) A review of groundwater arsenic contamination in Bangladesh: the millennium development goal era and beyond. Int J Environ Res Public Health 13(2):215. https://doi.org/10.3390/ijerph13020215

    Article  CAS  Google Scholar 

  4. WHO (2017) Guidelines for drinking-water quality: fourth edition incorporating the first addendum. World Health Organization, Geneva

    Google Scholar 

  5. IARC (2012) IARC monographs on the evaluation of carcinogenic risks to humans. Arsenic, metals, fibres, and dusts, vol 100C. Iarc Press, Lyon

    Google Scholar 

  6. EFSA (2009) Panel on contaminants in the food chain (CONTAM). Scientific opinion on arsenic in food. EFSA J 7(10):1351. https://doi.org/10.2903/j.efsa.2009.1351

    Article  Google Scholar 

  7. Borgoño JM, Vicent P, Venturino H, Infante A (1977) Arsenic in the drinking water of the city of Antofagasta: epidemiological and clinical study before and after the installation of a treatment plant. Environ Health Perspect 19:103–105. https://doi.org/10.1289/ehp.19-1637404

    Article  Google Scholar 

  8. Guha Mazumder D, Dasgupta UB (2011) Chronic arsenic toxicity: studies in West Bengal, India. Kaohsiung J Med Sci 27(9):360–370. https://doi.org/10.1016/j.kjms.2011.05.003

    Article  CAS  Google Scholar 

  9. Majumdar KK, Guha Mazumder DN, Ghose N, Ghose A, Lahiri S (2009) Systemic manifestations in chronic arsenic toxicity in absence of skin lesions in West Bengal. Indian J Med Res 129:75–82

    CAS  Google Scholar 

  10. Heywood R, Sortwell RJ (1978) Arsenic intoxication in the rhesus monkey. Toxicol Lett 3:137–144. https://doi.org/10.1016/0378-4274(79)90013-4

    Article  Google Scholar 

  11. Chiocchetti GM, Domene A, Kühl AA, Zúñiga M, Vélez D, Devesa V, Monedero V (2019a) In vivo evaluation of the effect of arsenite on the intestinal epithelium and associated microbiota in mice. Arch Toxicol 93:2127–2139. https://doi.org/10.1007/s00204-019-02510-w

    Article  CAS  Google Scholar 

  12. Calatayud M, Devesa V, Velez D (2013) Differential toxicity and gene expression in Caco-2 cells exposed to arsenic species. Toxicol Lett 218(1):70–80. https://doi.org/10.1016/j.toxlet.2013.01.013

    Article  CAS  Google Scholar 

  13. Calatayud M, Gimeno-Alcaniz JV, Devesa V, Velez D (2015) Proinflammatory effect of trivalent arsenical species in a co-culture of Caco-2 cells and peripheral blood mononuclear cells. Arch Toxicol 89(4):555–564. https://doi.org/10.1007/s00204-014-1271-1

    Article  CAS  Google Scholar 

  14. Calatayud M, Gimeno-Alcaniz JV, Velez D, Devesa V (2014) Trivalent arsenic species induce changes in expression and levels of proinflammatory cytokines in intestinal epithelial cells. Toxicol Lett 224(1):40–46. https://doi.org/10.1016/j.toxlet.2013.09.016

    Article  CAS  Google Scholar 

  15. Chiocchetti GM, Vélez D, Devesa V (2018) Effect of subchronic exposure to inorganic arsenic on the structure and function of the intestinal epithelium. Toxicol Lett 206:80–88. https://doi.org/10.1016/j.toxlet.2018.01.011

    Article  CAS  Google Scholar 

  16. Chiocchetti GM, Vélez D, Devesa V (2019b) Inorganic arsenic causes intestinal barrier disruption. Metallomics. https://doi.org/10.1039/C9MT00144A

  17. Groschwitz KR, Hogan SP (2009) Intestinal barrier function: molecular regulation and disease pathogenesis. J Allergy Clin Immunol 124(1):3–20. https://doi.org/10.1016/j.jaci.2009.05.038

    Article  CAS  Google Scholar 

  18. König J, Wells J, Cani PD, García-Ródenas CL, MacDonald T, Mercenier A, Whyte J, Troost F, Brummer R-J (2016) Human intestinal barrier function in health and disease. Clin Transl Gastroenterol 7(10):e196. https://doi.org/10.1038/ctg.2016.54

    Article  CAS  Google Scholar 

  19. Donato KA, Gareau MG, Wang YJ, Sherman PM (2010) Lactobacillus rhamnosus GG attenuates interferon-{gamma} and tumour necrosis factor-alpha-induced barrier dysfunction and pro-inflammatory signalling. Microbiology 156(Pt 11):3288–3297. https://doi.org/10.1099/mic.0.040139-0

    Article  CAS  Google Scholar 

  20. Ulluwishewa D, Anderson RC, McNabb WC, Moughan PJ, Wells JM, Roy NC (2011) Regulation of tight junction permeability by intestinal bacteria and dietary components. J Nutr 141(5):769–776. https://doi.org/10.3945/jn.110.135657

    Article  CAS  Google Scholar 

  21. Mazé A, Boël G, Zúniga M, Bourand A, Loux V, Yebra MJ, Monedero V, Correia K, Jacques N, Beaufils S (2010) Complete genome sequence of the probiotic Lactobacillus casei strain BL23. J Bacteriol 192(10):2647–2648. https://doi.org/10.1128/JB.00076-10

    Article  CAS  Google Scholar 

  22. Jadan-Piedra C, Chiocchetti GM, Clemente MJ, Velez D, Devesa V (2018) Dietary compounds as modulators of metals and metalloids toxicity. Crit Rev Food Sci Nutr 58(12):2055–2067. https://doi.org/10.1080/10408398.2017.1302407

    Article  CAS  Google Scholar 

  23. Das R, Das A, Roy A, Kumari U, Bhattacharya S, Haldar PK (2015) Beta-carotene ameliorates arsenic-induced toxicity in albino mice. Biol Trace Elem Res 164(2):226–233. https://doi.org/10.1007/s12011-014-0212-4

    Article  CAS  Google Scholar 

  24. Roy A, Das A, Das R, Haldar S, Bhattacharya S, Haldar PK (2014) Naringenin, a citrus flavonoid, ameliorates arsenic-induced toxicity in Swiss albino mice. J Environ Pathol Toxicol Oncol 33(3):195–204

    Article  Google Scholar 

  25. Kadirvel R, Sundaram K, Mani S, Samuel S, Elango N, Panneerselvam C (2007) Supplementation of ascorbic acid and alpha-tocopherol prevents arsenic-induced protein oxidation and DNA damage induced by arsenic in rats. Hum Exp Toxicol 26(12):939–946. https://doi.org/10.1177/0960327107087909

    Article  CAS  Google Scholar 

  26. Biswas J, Sinha D, Mukherjee S, Roy S, Siddiqi M, Roy M (2010) Curcumin protects DNA damage in a chronically arsenic-exposed population of West Bengal. Hum Exp Toxicol 29(6):513–524. https://doi.org/10.1177/0960327109359020

    Article  CAS  Google Scholar 

  27. Chiocchetti GM, Jadán-Piedra C, Monedero V, Zúñiga M, Vélez D, Devesa V (2019c) Use of lactic acid bacteria and yeasts to reduce exposure to chemical food contaminants and toxicity. Crit Rev Food Sci Nutr 59(10):1534–1545. https://doi.org/10.1080/10408398.2017.1421521

    Article  CAS  Google Scholar 

  28. Tian F, Zhai Q, Zhao J, Liu X, Wang G, Zhang H, Zhang H, Chen W (2012) Lactobacillus plantarum CCFM8661 alleviates lead toxicity in mice. Biol Trace Elem Res 150(1–3):264–271. https://doi.org/10.1007/s12011-012-9462-1

    Article  CAS  Google Scholar 

  29. Zhai Q, Wang G, Zhao J, Liu X, Tian F, Zhang H, Chen W (2013) Protective effects of Lactobacillus plantarum CCFM8610 against acute cadmium toxicity in mice. Appl Environ Microbiol 79(5):1508–1515. https://doi.org/10.1128/AEM.03417-12

    Article  CAS  Google Scholar 

  30. Halttunen T, Finell M, Salminen S (2007) Arsenic removal by native and chemically modified lactic acid bacteria. Int J Food Microbiol 120(1–2):173–178. https://doi.org/10.1016/j.ijfoodmicro.2007.06.002

    Article  CAS  Google Scholar 

  31. De Marco S, Sichetti M, Muradyan D, Piccioni M, Traina G, Pagiotti R, Pietrella D (2018) Probiotic cell-free supernatants exhibited anti-inflammatory and antioxidant activity on human gut epithelial cells and macrophages stimulated with LPS. Evid Based Complement Alternat Med 2018:1756308. https://doi.org/10.1155/2018/1756308

    Article  Google Scholar 

  32. Jeffrey MP, Strap JL, Jones Taggart H, Green-Johnson JM (2018) Suppression of intestinal epithelial cell chemokine production by Lactobacillus rhamnosus R0011 and Lactobacillus helveticus R0389 is mediated by secreted bioactive molecules. Front Immunol 9:2639. https://doi.org/10.3389/fimmu.2018.02639

    Article  CAS  Google Scholar 

  33. Tao Y, Drabik KA, Waypa TS, Musch MW, Alverdy JC, Schneewind O, Chang EB, Petrof EO (2006) Soluble factors from Lactobacillus GG activate MAPKs and induce cytoprotective heat shock proteins in intestinal epithelial cells. Am J Phys Cell Phys 290(4):C1018–C1030. https://doi.org/10.1152/ajpcell.00131.2005

    Article  CAS  Google Scholar 

  34. Zhai Q, Wang G, Zhao J, Liu X, Narbad A, Chen YQ, Zhang H, Tian F, Chen W (2014) Protective effects of Lactobacillus plantarum CCFM8610 against chronic cadmium toxicity in mice indicate routes of protection besides intestinal sequestration. Appl Environ Microbiol 80(13):4063–4071. https://doi.org/10.1128/AEM.00762-14

    Article  CAS  Google Scholar 

  35. 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(14):4429–4440. https://doi.org/10.1128/AEM.00695-16

    Article  CAS  Google Scholar 

  36. Bron PA, van Baarlen P, Kleerebezem M (2011) Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nat Rev Microbiol 10(1):66–78. https://doi.org/10.1038/nrmicro2690

    Article  CAS  Google Scholar 

  37. Segers ME, Lebeer S (2014) Towards a better understanding of Lactobacillus rhamnosus GG--host interactions. Microb Cell Factories 13(Suppl 1):S7. https://doi.org/10.1186/1475-2859-13-S1-S7

    Article  Google Scholar 

  38. Li H, Zhang L, Chen L, Zhu Q, Wang W, Qiao J (2016) Lactobacillus acidophilus alleviates the inflammatory response to enterotoxigenic Escherichia coli K88 via inhibition of the NF-kappaB and p38 mitogen-activated protein kinase signaling pathways in piglets. BMC Microbiol 16(1):273–278. https://doi.org/10.1186/s12866-016-0862-9

    Article  CAS  Google Scholar 

  39. Sun KY, Xu DH, Xie C, Plummer S, Tang J, Yang XF, Ji XH (2017) Lactobacillus paracasei modulates LPS-induced inflammatory cytokine release by monocyte-macrophages via the up-regulation of negative regulators of NF-kappaB signaling in a TLR2-dependent manner. Cytokine 92:1–11. https://doi.org/10.1016/j.cyto.2017.01.003

    Article  CAS  Google Scholar 

  40. Hsieh MH, Jan RL, Wu LS, Chen PC, Kao HF, Kuo WS, Wang JY (2018) Lactobacillus gasseri attenuates allergic airway inflammation through PPARgamma activation in dendritic cells. J Mol Med 96(1):39–51. https://doi.org/10.1007/s00109-017-1598-1

    Article  CAS  Google Scholar 

  41. Voltan S, Martines D, Elli M, Brun P, Longo S, Porzionato A, Macchi V, D'Inca R, Scarpa M, Palu G, Sturniolo GC, Morelli L, Castagliuolo I (2008) Lactobacillus crispatus M247-derived H2O2 acts as a signal transducing molecule activating peroxisome proliferator activated receptor-gamma in the intestinal mucosa. Gastroenterology 135(4):1216–1227. https://doi.org/10.1053/j.gastro.2008.07.007

    Article  CAS  Google Scholar 

  42. Karczewski J, Troost FJ, Konings I, Dekker J, Kleerebezem M, Brummer RJ, Wells JM (2010) Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. Am J Physiol Gastrointest Liver Physiol 298(6):G851–G859. https://doi.org/10.1152/ajpgi.00327.2009

    Article  CAS  Google Scholar 

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Acknowledgments

Gabriela de Matuoka e Chiocchetti received a fellowship from Brazilian Government (CAPES- BEX1086/14-6) to carry out this study.

Funding

This work was supported by the Spanish Ministry of Economy and Competitiveness (AGL2015-68920-R) and the Spanish Ministry of Science, Innovation and Universities (RTI2018-098071-B-I00), for which the authors are deeply indebted.

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Authors and Affiliations

  1. Instituto de Agroquímica y Tecnología de Alimentos (IATA-CSIC), C. Agustín Escardino 7, 46980, Valencia, Paterna, Spain

    Gabriela de Matuoka e Chiocchetti, Vicente Monedero, Manuel Zúñiga, Dinoraz Vélez & Vicenta Devesa

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  1. Gabriela de Matuoka e Chiocchetti
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  2. Vicente Monedero
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Correspondence to Vicenta Devesa.

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de Matuoka e Chiocchetti, G., Monedero, V., Zúñiga, M. et al. In Vitro Evaluation of the Protective Role of Lactobacillus StrainsAgainst Inorganic Arsenic Toxicity. Probiotics & Antimicro. Prot. 12, 1484–1491 (2020). https://doi.org/10.1007/s12602-020-09639-6

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