Induction of apoptosis in human T-cells by methyl mercury: Temporal relationship between mitochondrial dysfunction and loss of reductive reserve

Toxicology and Applied Pharmacology

Volumn 157, Issue 1, 1999, Pages 23-35

  Shenker, Bruce J ^a   Guo, Tai L ^a   Insug, O ^a   Shapiro, Irving M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Apoptosis; Immunotoxicity; Lymphocytes; Mercury; Mitochondrial permeability transition

Indexed keywords

CARDIOLIPIN; METHYLMERCURY;

APOPTOSIS; ARTICLE; AUTOIMMUNITY; CELL DEATH; CELL ORGANELLE; CYTOSOL; ELECTRON TRANSPORT; ENVIRONMENTAL EXPOSURE; HUMAN; HUMAN CELL; IMMUNOTOXICITY; MITOCHONDRIAL MEMBRANE; T LYMPHOCYTE ACTIVATION; TARGET CELL; TISSUE SPECIFICITY;

EID: 0033562940     PISSN: 0041008X     EISSN: None     Source Type: Journal    
DOI: 10.1006/taap.1999.8652     Document Type: Article

References (78)

1. Anderson M. E. Determination of glutathione disulfide in biological samples. Methods Enzymol. 113:1985;548-555.
2. Anderson P. Kinase cascades regulating entry into apoptosis. Microbiol. Mol. Biol. Rev. 61:1997;33-46.
3. Aschner M., Mullaney K. J., Wagoner D., Lash L. H., Kimelberg H. K. Intracellular glutathione (GSH) levels modulate mercuric chloride (MC)- and methylmercuric chloride (MeHgCl)-induced amino acid release from neonatal rat primary astrocytes cultures. Brain Res. 664:1994;133-140.
4. Atchison W. D., Hare M. F. Mechanisms of methylmercury-induced neurotoxicity. FASEB J. 8:1994;622-629.
5. Aten J., Prigent P., Poncet P., Blanpied C., Claessen N., Druet P., Hirsch F. Mercuric chloride-induced programmed cell death of a murine T cell hybridoma. 1. Effect of the proto-oncogene Bcl-2. Cell. Immunol. 161:1995;98-106.
6. Betti C., Davini T., He J., Barale R. Liquid holding effects on methylmercury genotoxicity in human lymphocytes. Mutat. Res. 301:1993;267-273.
7. Buttke T. M., Sandstrom P. A. Oxidative stress as a mediator of apoptosis. Immunol. Today. 15:1995;7-10.
8. Caron-Leslie L. M., Evans R. B., Cidlowski J. A. Bcl-2 inhibits glucocorticoid-induced apoptosis but only partially blocks calcium ionophore or cycloheximide-regulated apoptosis in S49 cells. FASEB J. 8:1994;639-645.
9. Castedo M., Hirsch F., Susin S. A., Zamzami N., Marchetti P., Macho A., Kroemer G. Sequential acquisition of mitochondrial and plasma membrane alterations during early lymphocyte apoptosis. J. Immunol. 157:1996;512-521.
10. Castedo M., Macho A., Zamzami N., Hirsch T., Marchetti P., Uriel J., Kroemer G. Mitochondrial perturbations define lymphocytes undergoing apoptotic depletionin vivo. Eur. J. Immunol. 25:1995;3277-3284.
11. o. J. Toxicol. Environ. Health. 52:1997;19-33.
12. Clarkson T. W. The toxicology of mercury. Crit. Rev. Clin. Lab. Sci. 34:1997;369-403.
13. Cohen G. M. Review article: Caspases: the executioners of apoptosis. Biochemistry. 326:1997;1-16.
14. Dantas D. C. M., Queiroz M. L. S. Immunoglobulin E and autoantibodies in mercury-exposed workers. Immunopharm. Immunotox. 19:1997;383-392.
15. De Flora S., Bennicelli C., Bagnasco M. Genotoxicity of mercury compounds. A review. Mutat. Res. 317:1994;57-79.
16. Descotes J., Nicholas B., Vial T. Assessment of immunotoxic effects in humans. Clin. Chem. 41:1995;1870-1873.
17. Dieter M. P., Luster M. I., Boorman G. A., Jameson C. W., Dean J. H., Cox J. W. Immunological and biochemical responses in mice treated with mercuric chloride. Toxicol. Appl. Pharmacol. 68:1983;218-228.
18. Fan A., Howd R., Davis B. Risk assessment of environmental chemicals. Annu. Rev. Pharmacol. Toxicol. 35:1995;341-368.
19. L. J. Immunol. 155:1995;66-75.
20. Foulkes E. C. Methallothionein and glutathione as determinants of cellular retention and extrusion of cadmium and mercury. Life Sci. 52:1993;1617-1620.
21. Franchi E., Loprieno G., Ballardin M., Petrozzi L., Migliore L. Cytogenetic monitoring of fishermen with environmental mercury exposure. Mutat. Res. 320:1994;23-29.
22. Furlong I. J., Ascaso R., Lopez R., Collins M. K. Intracellular acidification induces apoptosis by stimulating ICE-like protease activity. J. Cell Sci. 110:1997;653-661.
23. Gmunder H., Eck H.-P., Benninghoff B., Roth S., Droge W. Macrophages regulate intracellular glutathione levels of lymphocytes. Evidence for an immunoregulatory role of cysteine. Cell. Immunol. 129:1990;32-46.
24. Golstein P. Controlling cell death. Science. 275:1997;1081-1082.
25. Hamilton-Kock W., Snyder R., Lavelle J. Mental induced DNA damage and repair in human diploid fibroblasts and Chinese hamster ovary cells. Chem.-Biol. Interact. 59:1986;17-28.
26. Hansson M., Asea A., Ersson U., Hermodsson S., Hellstrand K. Induction of apoptosis in NK cells by monocyte-derived reactive oxygen metabolites. J. Immunol. 156:1996;42-47.
27. Heo Y., Lee W. T., Lawrence D. A. In vivo the environmental pollutants lead and mercury induce oligoclonal T cell responses skewed toward type-2 reactivities. Cell. Immunol. 179:1997;185-195.
28. Hirsch T., Marchetti P., Susin S. A., Dallaporta B., Zamzami N., Marzo I., Geuskens M., Kroemer G. The apoptosis-necrosis paradox. Apoptogenic proteases activated after mitochondrial permeability transition determine the mode of cell death. Oncogene. 15:1997;1573-1581.
29. Holsapple M. P., Karras J. G., Ledbetter J. A., Schieven G. L., Burchiel S. W., Davilla D. R., Schatz A. R., Kaminsky N. E. Molecular mechanisms of toxicant-induced immunosuppression: Role of second messengers. Annu. Rev. Pharmacol. Toxicol. 36:1996;131-159.
30. Houser M. T., Milner L. S., Kolbeck P. C., Wei S. H., Stohs S. J. Gluthione monoethyl ester moderates mercuric chloride-induced acute renal failure. Nephron. 61:1992;449-455.
31. Hu H., Moller G., Abedi-Valugerdi M. Thiol compounds inhibit mercury-induced immunological and immunopathological alterations in susceptible mice. Clin. Exp. Immunol. 107:1997;68-75.
32. Jacobson M. D., Raff M. C. Programmed cell death and Bcl-2 protection in very low oxygen. Nature. 374:1995;814-816.
33. o. Toxicology. 98:1995;67-72.
34. Kluck R. M., Bossy-Wetzel E., Green D. R., Newmeyer D. D. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science. 275:1997;1132-1136.
35. Kroemer G. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nature Med. 3:1997;614-620.
36. Kroemer G., Petit P., Zamzami N., Vayssiere J., Mignotte B. The biochemistry of programmed cell death. FASEB J. 9:1995;1277-1287.
37. Kroemer G., Zamzami N., Susin S. A. Mitochondrial control of apoptosis. Immunol. Today. 18:1997;44-51.
38. Krzystyniak K., Tryphonas H., Fournier M. Approaches to the evaluation of chemical-induced immunotoxicity. Environ. Health Perspect. 103:1995;17-22.
39. Langworth S., Sallsten G., Barregard L., Cynkier I., Lind M.-L., Soderman E. Exposure to mercury vapor and impact on health in the dental profession in Sweden. J. Dent. Res. 76:1997;1397-1404.
40. Lawrence D. Heavy metal modulation of lymphocyte activation. I. In vitro effects of heavy metals on primary humoral immune responses. Toxicol. Appl. Pharmacol. 57:1981;439-451.
41. Lin K.-T., Xue J.-Y., Sun F. F., Wong P. Y.-K. Reactive oxygen species participate in peroxynitrite-induced apoptosis in HL-60 cells. Biochem. Biophys. Res. Commun. 230:1997;115-119.
42. 2. Clin. Exp. Immunol. 110:1997;418-422.
43. Lorscheider F. L., Vimy M. J., Summers A. O., Zwiers H. The dental amalgam mercury controversy - inorganic mercury and the CNS; Genetic linkage of mercury and antibiotic resistances in intestinal bacteria. Toxicology. 97:1995;19-22.
44. Marchetti P., Hirsch T., Zamzami N., Castedo M., Decaudin D., Susin S. A., Masse B., Kroemer G. Mitochondrial permeability transition triggers lymphocyte apoptosis. J. Immunol. 157:1996;4830-4836.
45. Meisenholder G. W., Martin S. J., Green D. R., Nordberg J., Babior B. M. G. R. A. Events in apoptosis. Acidification is downstream of protease activation and Bcl-2 protection. J. Biol. Chem. 271:1996;16260-16266.
46. Michaelson J. H., McCoy J. P., Hirszel P., Bigazzi P. E. Mercury-induced autoimmune glomerulonephritis in inbred rats. I. Kinetics and species specificity of autoimmune responses. Surv. Synth. Path. Res. 4:1985;401-411.
47. O, I. Datar, S. Koch, C. J. Shapiro, I. M. Shenker, B. J. Mercuric compounds inhibit human monocyte function by inducing apoptosis: Evidence for formation of reactive oxygen species, development of mitochondrial membrane permeability transition and loss of reductive reserve, Toxicol. 124, 211, 224.
48. Osorio E., Toledano M., Bravo M., Osorio R. Short-term changes in lymphocytes after placement of silver amalgam restorations in healthy subjects. Dent. Mater. 11:1995;323-326.
49. Petit P. X., Susin S. A., Zamzami N., Mignotte B., Kroemer G. Mitochondria and programmed cell death: back to the future. FEBS Lett. 396:1996;7-13.
50. Petruccioli L., Turillazzi P. Serum immunoglobulin levels in monkeys treated with methylmercury. Drug Chem. Toxicol. 13:1990;297-307.
51. Reed J. C. Bcl-2 and the regulation of programmed cell death. J. Cell Biol. 124:1994;1-6.
52. Reers M., Smith T. W., Chen L. B. J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochemistry. 30:1991;4480-4486.
53. Reynolds J. E., Li J., Eastman A. Detection of apoptosis by flow cytometry of cells simultaneously stained for intracellular pH (carboxy SNARF-1) and membrane permeability (Hoechst 33342). Cytometry. 25:1996;349-357.
54. Rice G. C., Bump E. A., Shrieve D. C., Lee W., Kovacs M. Quantitative analysis of cellular glutathione by flow cytometry utilizing monochlorobimane: some applications to radiation and drug resistancein vitroin vivo. Cancer Res. 46:1986;6110-6118.
55. Rothe G., Valet G. Flow cytometric analysis of respiratory burst activity in phagocytres with hydroethidine and 2′,7′-dichlorofluorescin. J. Leuk. Bio. 47:1990;440-448.
56. Sandstrom P. A., Mannie M. D., Buttke T. M. Inhibition of activation-induced death in T cell hybridomas by thiol antioxidants: Oxidative stress as a mediator of apoptosis. J. Leukoc. Biol. 55:1994;221-226.
57. 2. Immunogenetics. 20:1984;227-236.
58. Schmid I., Uittenbogaart C. H., Giorgi J. V. Sensitive method for measuring apoptosis and cell surface phenotype in human thymocytes by flow cytometry. Cytometry. 15:1994;12-20.
59. Shenker B. J., Berthold P., Decker S., Mayro J. S., Rooney C., Vitale L. A., Shapiro I. M. Immunotoxic effects of mercuric compounds on human lymphocytes and monocytes. II. Alterations in cell viability. Immunopharm. Immunotox. 14:1992a;555-577.
60. Shenker B. J., Berthold P., Rooney C., Vitale L. A., DeBolt K., Shapiro I. M. Immunotoxic effects of mercuric compounds on human lymphocytes and monocytes. III. Alterations in B-cell function and viability. Immunopharm. Immunotox. 15:1993a;87-112.
61. Shenker B. J., Datar S., Mansfield K., Shapiro I. M. Induction of apoptosis in human T-cells by organomercuric compounds: A flow cytometric analysis. Toxicol. Appl. Pharmacol. 143:1997;397-406.
62. Shenker B. J., Mayro J. S., Rooney C., Vitale L. A., Shapiro I. M. Immunotoxic effects of mercuric compounds on human lymphocytes and monocytes. IV. Alterations in cellular glutathione content. Immunopharm. Immunotox. 15:1993b;273-290.
63. Shenker B. J., Rooney C., Vitale L. A., Shapiro I. M. Immunotoxic effects of mercuric compounds on human lymphocytes and monocytes. I. Suppression of T-cell activation. Immunopharm. Immunotox. 14:1992b;539-553.
64. Shenker B. J., Vitale L., King C. Actinobacillus actinomycetemcomitans. Cell. Immunol. 164:1995;36-46.
65. Shenker B. J., Guo T. L., Shapiro I. M. Low-level methylmercury exposure causes human T-cells to undergo apoptosis: Evidence of mitochondrial dysfunction. Environ. Res. 77:1998;149-159.
66. Skulachev V. P. Why are mitochondria involved in apoptosis? Permeability transition pores and apoptosis as selective mechanisms to eliminate superoxide-producing mitochondria and cell. FEBS Lett. 397:1996;7-10.
67. Soleo L., Vacca A., Vimercati L., Bruno S., Di Loreto M., Zocchetti C., Di Stefano R., Candilio G., Lasorsa G., Franco G., Foa V. Minimal immunological effects on workers with prolonged low exposure to inorganic mercury. Occupation. Environ. Med. 54:1997;437-442.
68. Stejskal V. D. M., Forsbeck M., Cederbrant K., Asteman O. Mercury-specific lymphocytes: An indication of mercury allergy in man. J. Clin. Immunol. 16:1996;31-40.
69. Thuvander A., Sundberg J., Oskarsson A. Immunomodulating effects after perinatal exposure to methylmercury in mice. Toxicology. 114:1996;163-175.
70. Tietze F. Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione: Application to mammalian blood and other tissues. Anal. Biochem. 27:1969;502-522.
71. Van Loveren H., Steerenberg P. A., Vos J. G. Early detection of immunotoxicity: From animal studies to human biomonitoring. Toxicol. Lett. 77:1995;73-80.
72. Wallace K. B., Eells J. T., Madeira V. M. C., Cortopassi G., Jones D. P. Symposium overview: Mitochondria-mediated cell injury. Fundam. Appl. Toxicol. 38:1997;23-37.
73. Wang Y., Sostman A., Roman R., Stribling S., Vigna S., Hannun Y., Raymond J., Fitz J. G. Metabolic stress opens K+ channels in hepatoma cells through a Ca2+- and protein kinase calpha-dependent mechanism. J. Biol. Chem. 271:1996;18107-18113.
74. 2. J. Oral Pathol. Med. 23:1994;441-445.
75. Wolfe J. T., Ross D., Cohen G. M. A role for metals and free radicals in the induction of apoptosis in thymocytes. FEBS Lett. 352:1994;58-62.
76. Yasutake A., Hirayama K. Acute effects of methylmercury on hepatic and renal glutathione metabolisms in mice. Arch. Toxicol. 68:1994;512-516.
77. Zamzami N., Marchetti P., Castedo M., Decaudin D., Macho A., Hirsch T., Susin S. A., Petit P. X., Mignotte B., Kroemer G. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182:1995;367-377.
78. Zhou P., Qian L., Kozopas K. M., Craig R. W. Mcl-1, a Bcl-2 family member, delays the death of hematopoietic cells under a variety of apoptosis-inducing conditions. Blood. 89:1997;630-643.