In vitro and in vivo effects of mercuric chloride on thymic endocrine activity, NK and NKT cell cytotoxicity, cytokine profiles (IL-2, IFN-γ, IL-6): Role of the nitric oxide-l-arginine pathway

International Immunopharmacology

Volumn 6, Issue 3, 2006, Pages 376-389

  Santarelli, Lory ^a   Bracci, Massimo ^a   Mocchegiani, Eugenio ^b  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b INRCA   (Italy)

Author keywords

Cytokines; Cytotoxicity; l arginine; Mercuric chloride; Nitric oxide; Thymulin; Thymus; Zinc

Indexed keywords

ARGININE; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 2; INTERLEUKIN 6; MERCURIC CHLORIDE; NITRATE; NITRIC OXIDE; NITRITE; THYMULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; DRUG EFFECT; DRUG INHIBITION; DRUG TISSUE LEVEL; INNATE IMMUNITY; MALE; MOUSE; NATURAL KILLER CELL; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; THYMUS FUNCTION;

ANIMALS; ARGININE; CELLS, CULTURED; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; INTERFERON-GAMMA; INTERLEUKIN-2; KILLER CELLS, NATURAL; KINETICS; MALE; MERCURIC CHLORIDE; MICE; MICE, INBRED BALB C; NITRATES; NITRIC OXIDE; NITRITES; ORGAN CULTURE TECHNIQUES; SIGNAL TRANSDUCTION; SPLEEN; T-LYMPHOCYTES; THYMIC FACTOR, CIRCULATING; THYMUS GLAND;

EID: 31044447512     PISSN: 15675769     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.intimp.2005.08.028     Document Type: Article

References (87)

1. W. Savino, and M. Dardenne Neuroendocrine control of thymus physiology Endocr Rev 21 2000 412 443
2. M. Dardenne, and W. Savino Control of thymus physiology by peptidic hormones and neuropeptides Immunol Today 15 1994 518 523
3. N. Fabris, E. Mocchegiani, and M. Provinciali Plasticity of neuroendocrine-thymus interactions during aging Exp Gerontol 32 1997 415 429
4. E. Mocchegiani, M. Muzzioli, and R. Giacconi Zinc, metallothioneins, immune responses, survival and ageing Biogerontology 1 2000 133 143
5. M.C. Dokhelar, T. Tursz, M. Dardenne, and J.F. Bach Effect of a synthetic thymic factor (facteur thymique serique) on natural killer cell activity in humans Int J Immunopharmacol 5 1983 277 282
6. M. Muzzioli, E. Mocchegiani, N. Bressani, P. Bevilacqua, and N. Fabris In vitro restoration by thymulin of NK activity of cells from old mice Int J Immunopharmacol 14 1992 57 61
7. G. Trinchieri Natural killer cells wear different hats: effector cells of innate resistance and regulatory cells of adaptive immunity and of hematopoiesis Semin Immunol 7 1995 83 88
8. J.A. Marsh, P.G. Merlino, and P. Staeheli The effects of triodothyronine and thymulin on avian NK cytolytic activity Int Immunopharmacol 9-10 2001 1823 1830
9. E. Mocchegiani, and M. Malavolta NK and NKT cell functions in immunosenescence Aging Cell 3 2004 177 184
10. E. Mocchegiani, R. Giacconi, C. Cipriano, N. Gasparini, G. Bernardini, and M. Malavolta The variations during the circadian cycle of liver CD1d-unrestricted NK1.1 + TCR gamma/delta+ cells lead to successful ageing. Role of metallothionein/IL-6/gp130/PARP-1 interplay in very old mice Exp Gerontol 39 2004 775 788
11. K.M. Pollard, and P. Hultman 1997 Effects of mercury on the immune system Met Ions Biol Syst 34 1988 421 440
12. C.L. Gaworski, and R.P. Sharma The effects of heavy metals on [3H]thymidine uptake in lymphocytes Toxicol Appl Pharmacol 46 1978 305 313
13. N.G. Ilback, J. Sundberg, and A. Oskarsson Methyl mercury exposure via placenta and milk impairs natural killer (NK) cell function in newborn rats Toxicol Lett 58 1991 149 158
14. S.H. Kim, V.J. Johnson, and R.P. Sharma Oral exposure to inorganic mercury alters T lymphocyte phenotypes and cytokine expression in BALB/c mice Arch Toxicol 77 2003 613 620
15. C. Dubey, B. Bellon, and P. Druet TH1 and TH2 dependent cytokines in experimental autoimmunity and immune reactions induced by chemicals Eur Cytokine Netw 2 1991 147 152
16. S.H. Kim, V.J. Johnson, and R.P. Sharma Mercury inhibits nitric oxide production but activates proinflammatory cytokine expression in murine macrophage: differential modulation of NF-kappaB and p38 MAPK signaling pathways Nitric Oxide 7 2002 67 74
17. K. Hirokawa, and Y. Hayashi Acute methyl mercury intoxication in mice-effect on the immune system Acta Pathol Jpn 30 1980 23 32
18. A. Thuvander, J. Sundberg, and A. Oskarsson Immunomodulating effects after perinatal exposure to methylmercury in mice Toxicology 114 1996 163 175
19. M. Valentino, L. Santarelli, E. Pieragostini, L. Soleo, and E. Mocchegiani In vitro inhibition of thymulin production in mercury-exposed thymuses of young mice Sci Total Environ 270 2001 109 112
20. L. Santarelli, M. Valentino, M. Bracci, V. Rapisarda, L. Soleo, and E. Mocchegiani Reversibility of thymulin production impairment by l-arginine supplementation in mice exposed to inorganic mercury Int J Immunopathol Pharmacol 17 2 Suppl 2004 123 128
21. T.L. Syversen Effects of methyl mercury on protein synthesis in vitro Acta Pharmacol Toxicol 49 1981 422 426
22. T.L. Syversen Effects of repeated dosing of methyl mercury on in vivo protein synthesis in isolated neurones Acta Pharmacol Toxicol 50 1982 391 397
23. M.M. Christensen, S. Ellermann-Eriksen, J. Rungby, and S.C. Mogensen Comparison of the interaction of methyl mercury and mercuric chloride with murine macrophages Arch Toxicol 67 1993 205 211
24. M.M. Christensen Histochemical localization of autometallographically detectable mercury in tissues of the immune system from mice exposed to mercuric chloride Histochem J 28 1996 217 225
25. S.H. Kim, and R.P. Sharma Cytotoxicity of inorganic mercury in murine T and B lymphoma cell lines: involvement of reactive oxygen species, Ca(2+) homeostasis, and cytokine gene expression Toxicol In Vitro 17 2003 385 395
26. J.S. Woods, C.A. Calas, L.D. Aicher, B.H. Robinson, and C. Mailer Stimulation of porphyrinogen oxidation by mercuric ion. I. Evidence of free radical formation in the presence of thiols and hydrogen peroxide Mol Pharmacol 38 1990 253 260
27. J.S. Woods, and M.E. Ellis Up-regulation of glutathione synthesis in rat kidney by methyl mercury. Relationship to mercury-induced oxidative stress Biochem Pharmacol 50 1995 1719 1724
28. G.S. Buzard, and K.S. Kasprzak Possible roles of nitric oxide and redox cell signaling in metal-induced toxicity and carcinogenesis: a review J Environ Pathol Toxicol Oncol 19 2000 179 199
29. S. Moncada, R.M. Palmer, and E.A. Higgs The biological significance of nitric oxide formation from l-arginine Biochem Soc Trans 17 1989 642 644
30. E. Mocchegiani, L. Cacciatore, M. Talarico, M. Lingetti, and N. Fabris Recovery of thymic hormone levels in cancer patients by lysine-arginine combination Int J Immunopharmacol 12 1990 365 371
31. E. Mocchegiani, M. Muzzioli, L. Santarelli, and N. Fabris Restoring effect of oral supplementation of zinc and arginine on thymic endocrine activity and peripheral immune functions in aged mice Arch Gerontol Geriatr Suppl 3 1992 267 276
32. B. Haggqvist, S. Havarinasab, E. Bjorn, and P. Hultman The immunosuppressive effect of methylmercury does not preclude development of autoimmunity in genetically susceptible mice Toxicology 208 2005 149 164
33. Society of Toxicology Guiding principles in the use of animals in toxicology. Adopted by the Society of Toxicology in July 1989 Toxicol Appl Pharmacol 2002 178
34. S. Nakatsuru, J. Oohashi, H. Nozaki, S. Nakada, and N. Imura Effect of mercurials on lymphocyte functions in vitro Toxicology 36 1985 297 305
35. J.M. Zdolsek, O. Soder, and P. Hultman Mercury induces in vivo and in vitro secretion of interleukin-1 in mice Immunopharmacology 28 1994 201 208
36. K.G. Park, P.D. Hayes, P.J. Garlick, H. Sewell, and O. Eremin Stimulation of lymphocyte natural cytotoxicity by l-arginine Lancet 16 1991 645 646
37. T. Itoh, S. Kasahara, and T. Mori A thymic epithelial cell line, IT-45R1, induces the differentiation of pre-thymic progenitor cells into post-thymic cells through direct contact Thymus 4 1982 69 75
38. E. Mocchegiani, L. Amadio, and N. Fabris Neuroendocrine-thymus interactions. I. In vitro modulation of thymic factor secretion by thyroid hormones J Endocrinol Invest 13 1990 139 147
39. M. Dardenne, W. Savino, M.C. Gagnerault, T. Itoh, and J.F. Bach Neuroendocrine control of thymic hormonal production. I. Prolactin stimulates in vivo and in vitro the production of thymulin by human and murine thymic epithelial cells Endocrinology 125 1989 3 12
40. B. Kurz, B. von Gaudecker, B. Krisch, and R. Mentlein Rat thymic epithelial cells in vitro and in situ: characterization by immunocytochemistry and morphology Cell Tissue Res 283 1996 221 229
41. T. Itoh Establishment of an epithelial cell line from rat thymus Am J Anat 156 1979 99 104
42. A.G. Castro, T.M. Hauser, B.G. Cocks, J. Abrams, S. Zurawski, and T. Churakova Molecular and functional characterization of mouse signaling lymphocytic activation molecule (SLAM): differential expression and responsiveness in Th1 and Th2 cells J Immunol 163 1999 5860 5870
43. M. Arredouani, P. Matthijs, E. Van Hoeyveld, A. Kasran, H. Baumann, and J.L. Ceuppens Haptoglobin directly affects T cells and suppresses T helper cell type 2 cytokine release Immunology 108 2003 144 151
44. J. Fan, P. Nishanian, E.C. Breen, M. McDonald, and J.L. Fahey Cytokine gene expression in normal human lymphocytes in response to stimulation Clin Diagn Lab Immunol 5 1998 335 340
45. E. Mocchegiani, G. Nisticò, L. Santarelli, and N. Fabris Effect of l-arginine on thymic function. Possible role of l-arginine:nitric oxide (NO) pathway Arch Gerontol Geriatr Suppl 4 1994 163 170
46. K. Olczyk, E.J. Kucharz, and A. Glowacki Influence of chronic mercury poisoning upon the connective tissue in rats. I. Effect of mercuric chloride on glycosaminoglycan levels in tissues, serum and urine Cent Eur J Public Health 2 1994 77 79
47. L. Soleo, A. Vacca, L. Vimercati, S. Bruno, M. Di Loreto, and C. Zocchetti Minimal immunological effects on workers with prolonged low exposure to inorganic mercury Occup Environ Med 54 6 1997 437 442
48. S. Enestrom, and P. Hultman Does amalgam affect the immune system? A controversial issue Int Arch Allergy Immunol 106 1995 180 203
49. P. Matthys, C. Dillen, P. Proost, H. Heremans, J. Van Damme, and A. Billiau Modification of the anti-CD3-induced cytokine release syndrome by anti-interferon-gamma or anti-interleukin-6 antibody treatment: protective effects and biphasic changes in blood cytokine levels Eur J Immunol 23 1993 2209 2216
50. J.M. Hevel, and M.A. Marletta Nitric-oxide synthase assays Methods Enzymol 233 1994 250 258
51. Y. Chen, and Z. Peng A sensitive in situ ELISA for quantitative measurements of cytokines and antibodies secreted by culture lymphocytes J Immunoassay Immunochem 22 2001 353 369
52. J.F. Bach, M. Dardenne, J.M. Pleau, and M.A. Bach Isolation, biochemical characteristics and biological activity of a circulating thymic hormone in the mouse and the human Ann NY Acad Sci USA 249 1975 186 210
53. E. Mocchegiani, L. Santarelli, M. Muzzioli, and N. Fabris Reversibility of the thymic involution and of age-related peripheral immune dysfunctions by zinc supplementation in old mice Int J Immunopharmacol 17 1995 703 718
54. N. Fabris, E. Mocchegiani, L. Amadio, M. Zannotti, F. Licastro, and C. Franceschi Thymic hormone deficiency in normal ageing and Down's syndrome: is there a primary failure of the thymus? Lancet 1 1984 983 986
55. H. Hu, G. Moller, and M. Abedi-Valugerdi Mechanism of mercury-induced autoimmunity: both T helper 1- and T helper 2-type responses are involved Immunology 96 1999 348 357
56. P. Bardos, and J.F. Bach Modulation of mouse natural killer cell activity by the serum thymic factor Scand J Immunol 16 1982 321 325
57. L.G. Wild, H.G. Ortega, M. Lopez, and J.E. Salvaggio Immune system alteration in the rat after indirect exposure to methyl mercury chloride or methyl mercury sulfide Environ Res 74 1997 34 42
58. D.R. Lucey, M. Clerici, and G.M. Shearer Type 1 and type 2 cytokine dysregulation in human infectious, neoplastic, and inflammatory diseases Clin Microbiol Rev 9 1996 532 562
59. P. Hultman, and S. Enestrom Mercury induced B-cell activation and antinuclear antibodies in mice J Clin Lab Immunol 28 1989 143 150
60. S. Havarinasab, B. Haggqvist, E. Bjorn, K.M. Pollard, and P. Hultman Immunosuppressive and autoimmune effects of thimerosal in mice Toxicol Appl Pharmacol 204 2005 109 121
61. Pelletier L, Pasquier R, Rossert J, Vial MC, Mandet C, Druet P. Autoreactive T cells in mercury-induced autoimmunity. Ability to induce the autoimmune disease. J Immunol. 1. 750-4.
62. L.L. Kosuda, D.L. Greiner, and P.E. Bigazzi Effects of HgCl2 on the expression of autoimmune responses and disease in diabetes-prone (DP) BB rats Autoimmunity 26 1997 173 187
63. P. Hultman, and U. Johansson Strain differences in the effect of mercury on murine cell-mediated immune reactions Food Chem Toxicol 29 1991 633 638
64. L. Jarup Hazards of heavy metal contamination Br Med Bull 68 2003 167 182
65. B. Haggqvist, and P. Hultman Effects of deviating the Th2-response in murine mercury-induced autoimmunity towards a Th1-response Clin Exp Immunol 134 2003 202 209
66. P. Hultman, and H. Hansson-Georgiadis Methyl mercury-induced autoimmunity in mice Toxicol Appl Pharmacol 154 1999 203 211
67. B. Rowley, and M. Monestier Mechanisms of heavy metal-induced autoimmunity Mol Immunol 42 2005 833 838
68. U. Johansson, B. Sander, and P. Hultman Effects of the murine genotype on T cell activation and cytokine production in murine mercury-induced autoimmunity J Autoimmun 10 1997 347 355
69. L.M. Bagenstose, P. Salgame, and M. Monestier Mercury-induced autoimmunity in the absence of IL-4 Clin Exp Immunol 114 1998 9 12
70. D.H. Kono, D. Balomenos, D.L. Pearson, M.S. Park, B. Hildebrandt, and P. Hultman The prototypic Th2 autoimmunity induced by mercury is dependent on IFN-gamma and not Th1/Th2 imbalance J Immunol 161 1998 234 240
71. P.H. van der Meide, R.J. Groenestein, M.C. de Labie, J. Aten, and J.J. Weening Susceptibility to mercuric chloride-induced glomerulonephritis is age-dependent: study of the role of IFN-gamma Cell Immunol 162 1995 131 137
72. V.K. Singh, S. Mehrotra, and S.S. Agarwal The paradigm of Th1 and Th2 cytokines: its relevance to autoimmunity and allergy Immunol Res 20 1999 147 161
73. S. Havarinasab, and P. Hultman Organic mercury compounds and autoimmunity Autoimmun Rev 4 2005 270 275
74. E. Mocchegiani, R. Giacconi, C. Cipriano, M. Muzzioli, N. Gasparini, and R. Moresi MtmRNA gene expression, via IL-6 and glucocorticoids, as potential genetic marker of immunosenescence: lessons from very old mice and humans Exp Gerontol 37 2002 349 357
75. G. Caspritz, and J. Hadden The immunopharmacology of immunotoxicology and immunorestoration Toxicol Pathol 15 1987 320 332
76. J.B. Nielsen, and P. Hultman Mercury-induced autoimmunity in mice Environ Health Perspect 110 Suppl 5 2002 877 881
77. M. Dardenne, J.M. Pleau, B. Nabarra, P. Lefrancier, M. Derrien, and J. Choay Contribution of zinc and other metals to the biological activity of the serum thymic factor Proc Natl Acad Sci U S A 79 1982 5370 5373
78. L.N. Gastinel, M. Dardenne, J.M. Pleau, and J.F. Bach Studies on the zinc binding site to the serum thymic factor Biochim Biophys Acta 797 1984 147 155
79. S. Nakada, K. Inoue, S. Nojima, and N. Imura Change in permeability of liposomes caused by methylmercury and inorganic mercury Chem Biol Interact 22 1978 15 23
80. B.J. Shenker, T.L. Guo, and I.M. Shapiro Mercury-induced apoptosis in human lymphoid cells: evidence that the apoptotic pathway is mercurial species dependent Environ Res 84 2000 89 99
81. T.A. Sarafian Methylmercury-induced generation of free radicals: biological implications Met Ions Biol Syst 36 1996 415 444
82. D. Quig Cysteine metabolism and metal toxicity Altern Med Rev 3 1998 262 270
83. S. Moncada, and E.A. Higgs Endogenous nitric oxide: physiology, pathology and clinical relevance Eur J Clin Invest 21 1991 361 374
84. R. Berkels, S. Purol-Schnabel, and R. Roesen Measurement of nitric oxide by reconversion of nitrate/nitrite to NO Methods Mol Biol 279 2004 1 8
85. L. Tian, and D.A. Lawrence Metal-induced modulation of nitric oxide production in vitro by murine macrophages: lead, nickel, and cobalt utilize different mechanisms Toxicol Appl Pharmacol 141 1996 540 547
86. M. Mori, and T. Gotoh Arginine metabolic enzymes, nitric oxide and infection J Nutr 134 2004 2820S 2825S
87. M. Colasanti, and H. Suzuki The dual personality of NO Trends Pharmacol Sci 21 2000 249 252