Toxicity of oral cadmium intake: Impact on gut immunity

Toxicology Letters

Volumn 237, Issue 2, 2015, Pages 89-99

  Ninkov, Marina ^a   Popov Aleksandrov, Aleksandra ^a   Demenesku, Jelena ^a   Mirkov, Ivana ^a   Mileusnic, Dina ^a   Petrovic, Anja ^a   Grigorov, Ilijana ^a   Zolotarevski, Lidija ^b   Tolinacki, Maja ^a   Kataranovski, Dragan ^a   Brceski, Ilija ^c   Kataranovski, Milena ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

^b UNIVERSITY OF DEFENCE   (Serbia)

^c UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

Intestinal (duodenum) inflammation; Mesenteric lymph nodes immune priming; Oral cadmium intake; Rats

Indexed keywords

BACTERIAL ANTIGEN; CADMIUM; CATALASE; CD68 ANTIGEN; GAMMA INTERFERON; GLUTATHIONE; HIGH MOBILITY GROUP B PROTEIN; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; MESSENGER RNA; METALLOTHIONEIN; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR; CYTOKINE;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE RESPONSE; IMMUNE RESPONSE; IMMUNITY; INNATE IMMUNITY; INTESTINE; LACTOBACILLUS; MALE; MESENTERY LYMPH NODE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; RAT; TISSUE INJURY; ANIMAL; BIOSYNTHESIS; CELL CULTURE; DRUG EFFECTS; IMMUNOLOGY; LYMPH NODE; METABOLISM; PATHOLOGY;

BACTERIA (MICROORGANISMS); LACTOBACILLUS; RATTUS;

ANIMALS; CADMIUM; CELL PROLIFERATION; CELLS, CULTURED; CYTOKINES; IMMUNITY, INNATE; INTESTINES; LYMPH NODES; MALE; RATS;

EID: 84931264431     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2015.06.002     Document Type: Article

References (76)

1. Andersen O., Nielsen J.B., Svendsen P. Oral cadmium chloride intoxication in mice: diethyldithiocarbamate enhances rather than alleviates acute toxicity. Toxicol 1988, 52:331-342.
2. Anderson M.E. Tissue glutathione. The DTNB-GSSG reductase recycling assay for total glutathione (GSH+1/2GSSG). Handbook of Methods for Oxigen Radical Research 1986, 317-323. CRC Press, Boca Raton, FL. R.A. Greenwald (Ed.).
3. Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat. Rev. Immunol. 2008, 8:411-420.
4. Asar M., Kayisli U.A., Izgut-Uysal V.N., Oner G., Kaya M., Polat S. Cadmium-induced changes in epithelial cells of the rat stomach. Biol. Trace Elem. Res. 2000, 77:65-81.
5. Bancroft G.J. The role of natural killer cells in inate resistance to infection. Curr. Opin. Immunol. 1993, 5:503-510.
6. Beutler E. Catalase. Red Cell Metabolism: A Manual of Biochemical Methods 1982, 105-106. Grune and Stratton, New York. E. Beutler (Ed.).
7. Bhattacharyya M.H., Whelton B.D., Peterson D.P., Carnes B.A., Moretti E.S., Toomey J.M., Williams L.L. Skeletal changes in multiparous mice fed a nutrient-sufficient diet containing cadmium. Toxicology 1988, 50:193-204.
8. Bjerke K., Halstensen T.S., Jahnsen F., Pulford K., Brandtzaeg P. Distribution of macrophages and granulocytes expressing L1 protein (calprotectin) in human Peyer's patches compared with normal ileal lamina propria and mesenteric lymph nodes. Gut 1993, 34:1357-1363.
9. Blanusa M., Mrkovic-Milic R., Durbesic P. Lead and cadmium in soil and Isopoda woodlice in Croatia. Ecotoxicol. Environ. Saf. 2002, 52:198-202.
10. Bozeman P.M., Learn D.B., Thomas E.L. Assay of the human leukocyte enzymes myeloperoxidase and eosinophil peroxidase. J. Immunol. Methods 1990, 126:125-133.
11. Breton J., Daniel C., Dewulf J., Pothion S., Froux N., Sauty M., Thomas P., Pot B., Foligne B. Gut microbiota limits heavy metals burden caused by chronic oral exposure. Toxicol. Lett. 2013, 222:132-138.
12. Breton J., Le Clere K., Daniel C., Sauty M., Nakab L., Chassat T., Dewulf J., Penet S., Carnoy C., Thomas P., Pot B., Nesslany F., Foligne B. Chronic ingestion of cadmium and lead alters the bioavailability of essential and heavy metals, gene expression pathways and genotoxicity in mouse intestine. Arch. Toxicol. 2013, 87:1787-1795.
13. Bron P.A., van Baarlen P., Kleerebezem M. Emerging molecular insigts into the interaction between probiotics and the host intestinal mucosa. Nat. Rev. Immunol. 2012, 10:66-78.
14. Chen G., Ward M.F., Sama A.E., Wang H. Extracellular HMGB1 as a proinflammatory cytokine. J. Interferon Cytokine Res. 2004, 24:329-333.
15. Chen G.Y., Nuñez G. Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 2010, 10:826-837.
16. Chen L., Xu B., Liu L., Luo Y., Zhou H., Chen W., Shen T., Han X., Kontos C.D., Huang S. Cadmium induction of reactive oxygen species activates mTOR pathway, leading to neuronal cell death. Free Radic. Biol. Med. 2011, 50:624-632.
17. Damek-Poprawa M., Sawicka-Kapusta K. Histopathological changes in the liver, kidneys, and testes of bank voles environmentally smelter in Poland. Environ. Res. 2004, 96:72-78.
18. Demenesku J., Mirkov I., Ninkov M., Popov-Aleksandrov A., Zolotarevski L., Kataranovski D., Kataranovski M. Acute cadmium administration to rats exerts both immunosuppressive and proinflammatory effects in spleen. Toxicol 2014, 326:96-108.
19. Fazeli M., Hassanzadeh P., Alaei S. Cadmium chloride exhibits a profound toxic effect on bacterial microflora of the mice gastrointestinal tract. Hum. Exp. Toxicol. 2011, 30:152-159.
20. Goon D., Klaassen C.D. Dosage-dependent absorption of cadmium in the rat intestine measured in situ. Toxicol. Appl. Pharmacol. 1989, 100:41-50.
21. Green D.R., Ferguson T., Zitvogel L., Kroemer G. Immunogenic and tolerogenic cell death. Nat. Rev. Immunol. 2009, 9:353-363.
22. Heilig H.G., Zoetendal E.G., Vaughan E.E., Marteau P., Akkermans A.D., de Vos W.M. Molecular diversity of Lactobacillus spp. and other lactic acid bacteria in the human intestine by specific amplification of 16S ribosomal DNA. Appl. Environ. Microbiol. 2002, 68:114-123.
23. Hibbs J.B., Taintor R.R., Vavrin Z., Rachlin E.M. Nitric oxide: a cytotoxic activated macrophage effector molecule. Biochem. Biophys. Res. Commun. 1988, 157:87-94.
24. Horiguchi H., Harada A., Oguma E., Sato M., Homma Y., Kayama F., Fukushima M., Matsushima K. Cadmium-induced acute hepatic injury is exacerbated in human interleukin-8 transgenic mice. Toxicol. Appl. Pharmacol. 2000, 163:231-239.
25. Hyun J.S., Satsu H., Shimizu M. Cadmium induces Interleukin-8 production via NF-kB activation in the human intestinal epithelial cell, Caco-2. Cytokine 2007, 37:26-34.
26. Jovanovic D.V., Di Battista J.A., Martel-Pelletier J., Jolicoeur F.C., He Y., Zhang M., Mineau F., Pelletier J.P. IL-17 stimulates the production and expression of proinflammatory cytokines, IL-beta and TNF-alpha, by human macrophages. J. Immunol. 1998, 160:3513-3521.
27. Kaplan M., Atakan I.H., Aydogdu N., Aktoz T., Ozpuyan F., Seren G., Tokuc B., Inci O. Influence of N-acetylcysteine on renal toxicity of cadmium in rats. Pediatr. Nephrol. 2008, 23:233-241.
28. Kawai Y., Suegara N. Specific adhesion of lactobacilli to keratinized epithelial cells of the rat stomach in vitro. Am. J. Clin. Nutr. 1977, 30:1777-1780.
29. Kayama F., Yoshida T., Elwell M.R., Luster M.I. Role of tumor necrosis factor-alpha in cadmium-induced hepatotoxicity. Toxicol. Appl. Pharmacol. 1995, 131:224-234.
30. Kayama F., Yoshida T., Elwell M.R., Luster M.I. Cadmium-induced renal damage and proinflammatory cytokines: possible role of IL-6 in tubular epithelial cell regeneration. Toxicol. Appl. Pharmacol. 1995, 134:26-34.
31. Klaassen C.D., Liu J., Diwan B.A. Metallothionein protection of cadmium toxicity. Toxicol. Appl. Pharmacol. 2009, 238:215-220.
32. Lalor G.C. Review of cadmium transfers from soil to humans and its health effects and Jamaican environment. Sci. Total Environ. 2008, 400:162-172.
33. Liu Y., Li Y., Liu K., Shen J. Exposing to cadmium stress cause profpund toxic effect on microbiota of the mice intestinal tract. PLoS ONE 2014, 10.1371/journal.pone.0085323.
34. López E., Figueroa S., Oset-Gasque M.J., González M.P. Apoptosis and necrosis: two distinct events induced by cadmium in cortical neurons in culture. Br. J. Pharmacol. 2003, 138:901-911.
35. Lowry O.H., Rosenbrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
36. Lukacinova A., Racz O., Lovasova E., Nistiar F. Effect of lifetime low dose exposure to heavy metals on selected serum proteins of Wistar rats during three subsequent generations. Ecotoxicol. Environ. Saf. 2011, 74:1747-1755.
37. Lukic J., Strahinic I., Milenkovic M., Golic N., Kojic M., Topisirovic L.J., Begovic J. Interaction of Lactobacillus fermentum BGHI14 with rat colonic mucosa: implications for colitis induction. Appl. Environ. Microbiol. 2013, 79:5735-5744.
38. MacPherson A.J., Smith K. Mesenteric lymph nodes at the center of immune anatomy. J. Exp. Med. 2006, 203:497-500.
39. Mane J., Loren V., Pedrosa E., Ojanguren I., Xaus J., Cabre E., Domenech E., Gassull M.A. Lactobacillus fermentum CECT 5716 prevents and reverts intestinal damage on TNBS-induced colitis in mice. Inflamm. Bowel Dis. 2009, 15:1155-1163.
40. Marth E., Jelovcan S., Kleinhappl B., Gutschi A., Barth S. The effect of heavy metals on the immune system at low concentrations. Int. J. Occup. Med. Environ. Health 2001, 14:375-386.
41. Martin-Fontecha A., Thomsen L.L., Brett S., Gerard C., Lipp M., Lanzavecchia A., Sallusto F. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H) 1 priming. Nat. Immunol. 2004, 5:1260-1265.
42. Mendieta-Wejebe J.E., Miliar-Garcia A., Correa-Basurto J., Sanchez-Rico C., Ramirez-Rosales D., Trujillo-Ferrara J., Rosales-Hernandez M.C. Comparison of the effect of chronic cadmium exposure on the antioxidant defense systems of kidney and brain in rat. Toxicol. Mech. Methods 2013, 23:329-336.
43. Mills C.D., Kincaid K., Alt J.M., Heilman M.J., Hill A.M. M-1/M-2 macrophages and the Th1/Th2 paradigm. J. Immunol. 2000, 164:6166-6173.
44. Misra H.P., Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J. Biol. Chem. 1972, 247:3170-3175.
45. Molin G., Jeppsson B., Johansson M.L., Ahrne S., Nobaek S., Stahl M., Benqmark S. Numerical taxonomy of Lactobacillus spp. Associated with healthy and diseased mucosal of the human intestines. J. Appl. Bacteriol. 1993, 74:314-323.
46. Molin G., Johansson M.L., Stahl M., Ahrne S., Andersson R., Jeppsson B., Bengmark S. Systematics of the Lactobacillus population on rat intestinal mucosa with special reference to Lactobacillus reuteri. Antonie van Leeuwenhoek 1992, 61:175-183.
47. Mowat A.M. Anatomical basis of tolerance and immunity to intestinal antigens. Nat. Rev. Immunol. 2003, 3:331-341.
48. Nordberg G.F. Historical perspectives on cadmium toxicology. Toxicol. Appl. Pharmacol. 2009, 238:192-200.
49. Nordberg M., Nordberg G.F. Toxicological aspects of metallothionein. Cell. Mol. Biol. (Noisy-le-Grand) 2000, 46:451-463.
50. Park J.D., Cherrington N.J., Klaassen C.D. Intestinal absorption of cadmium is associated with divalent metal transporter 1 in rats. Toxicol. Sci. 2002, 68:288-294.
51. Prozialeck W.C. Evidence that E-cadherin may be a target for cadmium toxicity in epithelial cells. Toxicol. Appl. Pharmacol. 2000, 164:231-249.
52. Rahman I., MacNee W. Regulation of redox glutathione levels and gene transcription in lung inflammation: therapeutic approaches. Free Radic. Biol. Med. 2000, 28:1405-1420.
53. Rana S.V., Verma S. Protective effects of GSH, vitamin E and selenium on lipid peroxidation in cadmium-fed rats. Bio. Trace. Elem. Res. 1996, 51:161-168.
54. Rikans L.E., Yamano T. Mechanisms of cadmium-mediated acute hepatotoxicity. J. Biochem. Mol. Toxicol. 2000, 14:110-117.
55. Rock K.L., Kono H. The inflammatory response to cell death. Annu. Rev. Pathol. 2008, 3:99-126.
56. Rutgveit J., Brandtzaeg P., Halstensen T.S., Fausa O., Scott H. Increased macrophage subset in inflammatory bowel disease: apparent recruitment from peripheral blood monocytes. Gut 1994, 35:669-674.
57. Sakuraba A., Sato T., Kamada N., Kitazume M., Sugita A., Hibi T. Th1/Th17 immune response is induced by mesenteric lymph node dendritic cells in Crohn's disease. Gastroenterol 2009, 137:1736-1745.
58. Sarra M., Pallone F., Macdonald T.T., Monteleone G. IL-23/IL-17 axis in IBD. Inflamm. Bowel Dis. 2010, 16:1808-1813.
59. Satarug S., Garrett S.H., Sens M.A., Sens D.A. Cadmium, environmental exposure, and health outcomes. Environ. Health Perspect. 2010, 118:182-190.
60. Scaffidi P., Misteli T., Bianchi M.E. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002, 418:191-195.
61. Shaikh Z.A., Vu T.T., Zaman K. Oxidative stress as a mechanism of chronic cadmium-induced hepatotoxicity and renal toxicity and protection by antioxidants. Toxicol. Appl. Pharmacol. 1999, 154:256-263.
62. Sherwood E.R., Toliver-Kinsky T. Mechanisms of the inflammatory response. Best Pract. Res. Clin. Anaesthesiol. 2004, 18:385-405.
63. Slack E., Hapfelmeier S., Stecher B., Velykoredko Y., Stoel M., Lawson M.A., Geuking M.B., Beutler B., Tedder T.F., Hardt W.D., Bercik P., Verdu E.F., McCoy K.D., MacPherson A.J. A flexible continuum between adaptive and innate immunity in maintaining host-microbiota mutualism. Science 2009, 325:617-620.
64. Stadnyk A.W. Intestinal epithelial cells as a source of inflammatory cytokines and chemokines. Can. J. Gastroenterol. 2002, 16:241-246.
65. Theocharis S.E., Souliotis V.L., Panayiotidis P.G. Suppression of interleukin-1 beta and tumour necrosis factor-alpha biosynthesis by cadmium in in vitro activated human peripheral blood mononuclear cells. Arch. Toxicol. 1994, 69:132-136.
66. Valberg L.S., Haist J., Cherian M.G., Delaquerriere-Richardson L., Goyer R.A. Cadmium-induced enteropathy: comparative toxicity of cadmium chloride and cadmium-thionein. Toxicol. Environ. Health 1977, 2:963-975.
67. Waeytens A., De Vos M., Laukens D. Evidence for a potential role of metallothioneins in inflammatory bowel disease. Mediators Inflamm. 2009, 10.1155/2009/729172.
68. Walrand S., Valeix S., Rodriguez C., Ligot P., Chassagne J., Vasson M.P. Flow cytometry study of polymorphonuclear neutrophil oxidative burst: a comparison of three fluorescent probes. Clin. Chim. Acta 2003, 331:103-110.
69. Wang H., Zhu G., Shi Y., Weng S., Jin T., Kong Q., Nordberg G.F. Influence of environmental cadmium exposure on forearm bone density. J. Bone Miner. Res. 2003, 18:553-560.
70. Wang L., Chen D., Cao J., Liu Z. Protective effect of N-acetylcysteine on experimental chronic cadmium nephrotoxicity in immature female rats. Hum. Exp. Toxicol. 2009, 28:221-229.
71. Weaver C.T., Hatton R.D., Mangan P.R., Harrington L.E. IL-17 family of 24 cytokines and the expanding diversity of effector T cell lineages. Annu. Rev. Immunol. 2007, 25:821-852.
72. WHO Environmental Health Criteria 134, Cadmium 1992, World Health Organization, Geneva, Switzerland. first ed.
73. Xu B., Chen S., Luo Y., Chen Z., Liu L., Zhou H., Chen W., Shen T., Han X., Chen L., Huang S. Calcium signaling is involved in cadmium-induced neuronal apoptosis via induction of reactive oxygen species and activation of MAPK/mTOR network. PLoS ONE 2011, 6:19052. 10.1371/journal.pone.0019052.
74. Yamada Y.K., Shimizu F., Kawamura R., Kubota K. Thymic atrophy in mice induced by cadmium administration. Toxicol. Lett. 1981, 8:49-55.
75. Yen D., Cheung J., Scheerens H., Poulet F., McClanahan T., McKenzie B., Kleinschek M.A., Owyang A., Mattson J., Blumenschein W., Murphy E., Sathe M., Cua D.J., Kastelein R.A., Rennick D. IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J. Clin. Invest. 2006, 116:1310-1316.
76. Zhao Z., Hyun J.S., Satsu H., Kakuta S., Shimizu M. Oral exposure to cadmium chloride triggers an acute inflammatory response in the intestines of mice, initiated by the over-expression of tissue macrophage inflammatory protein-2 mRNA. Toxicol. Lett. 2006, 164:144-154.