Stress proteins as agents of immunological change: Some lessons from metallothionein

Cell Stress and Chaperones

Volumn 1, Issue 2, 1996, Pages 99-108

  Borghesi, Lisa A ^a   Lynes, Michael A ^b  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN; METALLOTHIONEIN;

ANIMAL; HUMAN; IMMUNOLOGY; REVIEW;

ANIMALS; HEAT-SHOCK PROTEINS; HUMANS; METALLOTHIONEIN;

EID: 0030154445     PISSN: 13558145     EISSN: None     Source Type: Journal    
DOI: 10.1379/1466-1268(1996)001<0099:SPAAOI>2.3.CO;2     Document Type: Review

References (113)

1. Andersen R, Piletz J, Birren B and Herschman H (1983) Levels of metallothionein messenger RNA in fetal, neonatal and maternal rat liver. Eur. J. Biochem. 131, 497-500.
2. Andrews GK (1990) Regulation of metallothionein gene expression. Prog. Food Nutr. Sci. 14, 193-258.
3. Banerjee D, Onosaka S and Cherian G (1982) Immunohistochemical localization of metallothionein in cell nucleus and cytoplasm of rat liver and kidney. Toxicology 24, 95-105.
4. Bigazzi P (1988) Autoimmunity induced by chemicals. J. Toxicol. Clin. Toxicol. 26, 125-156.
5. Borghesi L, Youn J, Olson E and Lynes M (1996) Interactions of metallothionein with murine lymphocytes: Plasma membrane binding and proliferation. Toxicology 108, 129-140.
6. Brady F (1982) The physiological function of metallothionein. TIBS 7, 143-145.
7. Carter A, Felber B, Walling M, Jubier M-F, Schmidt C and Hamer D (1984) Duplicated heavy metal control sequences of the mouse metallothionein-I gene. Proc. Natl. Acad. Sci. USA 81, 7392-7396.
8. Chan H, Satoh M, Zalups R and Cherian M (1992) Exogenous metallothionein and renal toxicity of cadmium and mercury in rats. Toxicology 76, 15-26.
9. Cherian G, Huang P, Klaassen C, Liu Y-P, Longfellow D and Waalkes M (1993) National Cancer Institute workshop on the possible roles of metallothionein in carcinogenesis. Cancer Res. 53, 922-925.
10. Choudhuri S, McKim Jr. J and Klaassen C (1993) Differential expression of the metallothionein gene in liver and brain of mice and rats. Toxicol. Appl. Pharmacol. 119, 1-9.
11. Chubatsu L and Meneghini R (1993) Metallothionein protects DNA from oxidative damage. Biochem. J. 291, 193-198.
12. Churchich J, Scholz G and Kwok F (1989) Activation of pyridoxal kinase by metallothionein. Biochim. Biophys. Acta 996, 181-186.
13. Cousins R and Leinart A (1988) Tissue-specific regulation of zinc metabolism and metallothionein genes by inteileukin-1. FASEB J. 2, 2884-2890.
14. Daston G, Overmann G, Taubeneck M, Lehman-McKeeman L, Rogers J and Keen C (1991) The role of metallothionein induction and altered zinc status in maternally mediated developmental toxicity: comparison of the effects of urethane and styrene in rats. Toxicol. Appl. Pharmacol. 110, 450-463.
15. DiSilvestro RA and Carlson GP (1992) Inflammation, an inducer of metallothionein, inhibits carbon-tetrachloride-induced hepatotoxicity in rats. Toxicol. Lett. 60, 175-181.
16. Dorian C, Gattone V and Klaassen C (1995) Discrepancy between the nephrotoxic potencies of cadmium-metallothionein and cadmium chloride and the renal concentration of cadmium in the proximal convoluted tubules. Toxicol. Appl. Pharmacol. 130, 161-168.
17. Dudley R, Gammal L and Klaassen C (1985) Cadmium-induced hepatic and renal injury in chronically exposed rats: likely role of hepatic cadmium-metallothionein in nephrotoxicity. Toxicol. Appl. Pharmacol. 77, 414-426.
18. Durnam DM and Palmiter RD (1981) Transcriptional regulation of the mouse metallothionein-I gene by heavy metals. J. Biol. Chem. 256, 5712-5716.
19. Dumam DM, Hoffman JS, Quaife CJ, Benditt EP, Chen HY, Brinster RL and Palmiter RD (1984) Induction of mouse metallothionein-I mRNA by bacterial endotoxin is independent of metals and glucocorticoid hormones. Proc. Natl. Acad. Sci. USA 81, 1053-1056.
20. Erickson JC, Sewell AK, Jensen LT, Winge DR and Palmiter RD (1994) Enhanced neurotrophic activity in Alzheimer's disease cortex is not associated with down-regulation of metallothionein-III (GIF). Brain Res. 649, 297-304.
21. Falck F, Fine L, Smith R, et al (1983) Metallothionein and occupational exposure to cadmium. Br. J. Indust. Med. 40, 305-313.
22. Furey W, Robbins A, Clancy L, Winge D, Wang B and Stout C (1986) Crystal structure of Cd,Zn-metallothionein. Science 231, 704-710.
23. Gallant K and Cherian M (1989) Metabolic changes in glutathione and metallothionein in newborn rat liver. J. Pharmacol. Exper. Therap. 249, 631-637.
24. Garvey J (1984) Metallothionein: structure/antigenicity and detection/quantitation in normal physiological fluids. Env. Health Perspect. 54, 117-127.
25. Garvey J and Chang C (1981) Detection of circulating metallothionein in rats injected with zinc or cadmium. Science 214, 805-807.
26. Giralt M, Armario A and Hidalgo J (1993) Chronic stress reduces serum but not liver metallothionein response to acute stress. Chem. Biol. Interac. 88, 1-5.
27. Glanville N, Durnam D and Palmiter R (1981) Structure of mouse metallothionein-I gene and its mRNA. Nature 292, 267-268.
28. Goering P and Klaassen C (1983) Altered subcellular distribution of cadmium following cadmium pretreatment: possible mechanism of tolerance to cadmium-induced lethality. Toxicol. Appl. Pharmacol. 70, 195-203.
29. Hahn S, Brantly M, Oliver C, Adamson M, Kaler S and Gahl W (1994) Metallothionein synthesis and degradation in Indian Childhood Cirrhosis fibroblasts. Pediatr. Res. 35, 197-204.
30. Halliwell B and Aruoma OI (1991) DNA damage by oxygen-derived species: its mechanism and measurement in mammalian systems. FEBS Lett. 281, 9-19.
31. Hamer D (1986) Metallothionein. Ann. Rev. Biochem. 55, 913-951.
32. Harley C, Menon C, Rachubinski R and Nieboer E (1989) Metallothionein mRNA and protein induction by cadmium in peripheral-blood leukocytes. Biochem. J. 262, 873-879.
33. Hemps MH, Carlson JM and Cousins RJ (1991) Intestinal metallothionein gene expression and zinc absorption in rats are zinc-responsive but refractory to dexamethasone and interleukin-1a. J. Nutr. 121, 1389-1396.
34. Heuchel R, Radtke F, Georgiev O, Stark G, Aguet M and Schaffner W (1994) The transcription factor MTF-1 is essential for basal and heavy metal-induced metallothionein gene expression. EMBO J. 13, 2870-2875.
35. Hidalgo J, Armario A, Flos R and Garvey JS (1986) Restraint stress induced changes in rat liver and serum metallothionein and in Zn metabolism. In: Metallothionein II. Experientia Supplementum, eds J Kagi and Y Kojima, Birkhauser Verlag, Basel, 1006-1010.
36. Hidalgo J, Giralt M, Garvey JG and Armario A (1988) Physiological role of glucocorticoids on rat serum and liver metallothionein in basal and stress conditions. Am. J. Physiol 254, E71-E78.
37. Hightower L and Guidon P (1989) Selective release from cultured mammalian cells of heat-shock (stress) proteins that resemble glia-axon transfer proteins. J. Cell. Physiol. 138, 257-266.
38. Huang I-Y, Yoshida A, Tsunoo H and Nakajima H (1977) Mouse liver metallothioneins. Complete amino acid sequence of metallothionein-I. J. Biol. Chem. 252, 8217-8221.
39. Huerta P, Galan P, Teijon JM and Ribas B (1989) Increase of metallothionein and other proteins in thymus and spleen during chronic zinc administration. Toxic Env. Chem. 25, 63-68.
40. Hunt D, Wake S, Mercer J and Danks D (1986) A study of the role of metallothionein in the inherited copper toxicosis of dogs. Biochem. J. 236, 409-415.
41. Hunziker P and Kagi J (1985) Isolation and characterization of six human hepatic isometallothioneins. Biochem. J. 231, 375-382.
42. John T, Smith H, Fried V and Weissman I (1986) Cell surface molecule associated with lymphocyte homing is a ubiqutinated branched chain glycoprotein. Science 231, 823-829.
43. Kagi J and Schaffer A (1988) Biochemistry of metallothionein. Biochemistry 27, 8509-8515.
44. Karin M (1985) Metallothionein: proteins in search of a function. Cell 41, 9-10.
45. Karin M and Richards R (1982) Human metallothionein genes-primary structure of the metallothionein-II gene and a related processed gene. Nature 299, 797-802.
46. Karin M, Eddy R, Henry W, Haley L, Byers M and Shows T (1984) Human metallothionein genes are clustered on chromosome 16. Proc. Natl. Acad. Sci. USA 81, 5494-5498.
47. Karin M, Imbra R, Heguy A and Wong G (1985) Interleukin 1 regulates human metallothionein gene expression. Mol. Cell. Biol. 5, 2866-2869.
48. Kaufmann S (1994) Heat shock proteins and autoimmunity: a critical appraisal. Int. Arch. Allergy Immunol. 103, 317-322.
49. Kerkvliet N and Baecher-Stephenson L (1982) Immunotoxicology stuies on lead: effects of exposure on tumor growth and cell mediated tumor immunity after syngeneic or allogeneic stimulation. Immunopharmacology 4, 213-224.
50. Klaassen C and Lehman-McKeeman L (1989) Induction of metallothionein. J. Am. Coll. Toxicol. 8, 1315-1321.
51. Kondo Y, Woo E, Michalska A, Choo K and Lazo J (1995) Metallothionein null cells have increased sensitivity to anticancer drugs. Cancer Res. 55, 2021-2023.
52. Koropatnick J and Cherian M (1993) A mutant mouse (tx) with increased hepatic metallothionein stability and accumulation. Biochem. J. 296, 443-449.
53. Koropatnick J and Cherian M (1994) Metallothionein protein and mRNA in the toxic milk mouse. Biochem. J. 304, 318-319.
54. Koyama H, Satoh H, Suzuki S and Tohyama C (1992) Increased urinary cadmium excretion and its relationship to urinary N-acetyl-b-D-glucosaminidase activity in smokers. Arch. Toxicol. 66, 598-601.
55. Kuo S-M, Kondo Y, DeFilippo J, Ernstoff M, Bahnson R and Lazo J (1994) Subcellular localization of a metallothionein IIA in human bladder tumor cells using a novel epitope-specific antiserum. Toxicol. Appl. Pharmacol. 125, 104-110.
56. Labbe S, Larouche L, Mailhot D and Seguin C (1993) Purification of mouse MEP-1, a nuclear protein which binds to the metal regulatory elements of genes encoding metallothionein. Nucleic Acids Res. 21, 1549-1554.
57. Lawrence D (1981) In vivo and in vitro effects of lead on humoral and cell mediated immunity. Infect. Immun. 31, 136-144.
58. Lazo J, Kondo Y, Dellapiazza D, Michalska A, Choo K and Pitt B (1995) Enhanced sensitivity to oxidative stress in cultured embryonic cells from transgenic mice deficient in metallothionein I and II genes. J. Biol. Chem. 270, 5506-5510.
59. Leibbrandt M and Koropatnick J (1994) Activation of human monocytes with lipopolysaccharide induces metallothionein expression and is diminished by zinc. Toxicol. Appl. Pharmacol. 124, 72-81.
60. Leibbrandt M, Khokha R and Koropatnick J (1994) Antisense down-regulation of metallothionein in a human monocytic cell line alters adherence, invasion and the respiratory burst. Cell Growth Differ. 5, 17-25.
61. Leone A, Pavlakis G and Hamer D (1985) Menkes' disease: abnormal metallothionein gene regulation in response to copper. Cell 40, 301-309.
62. Li T-Y, Kraker A, Shaw III C and Petering D (1980) Ligand substitution reactions of metallothioneins with EDTA and apo-carbonic anhydrase. Proc. Natl. Acad. Sci. USA 77, 6334-6338.
63. Lynes M, Garvey J and Lawrence D (1990) Extracellular metallothionein effects on lymphocyte activities. Mol. Immunol. 27, 211-219.
64. Lynes M, Borghesi L, Youn J and Olson E (1993) Immunomodulatory activities of extracellular metallothionein I. Metallothionein effects on antibody production. Toxicology 85, 165-177.
65. Margeli A, Theocharis S, Yannacou N, Spiliopoulou C and Koutselinis A (1994) Metallothionein expression during liver regeneration after partial hepatectomy in cadmium-pretreated rats. Arch. Toxicol. 68, 637-642.
66. Margoshes M and Vallee B (1957) A cadmium binding protein from equine kidney cortex. J. Am. Chem. Soc. 79, 4813-4814.
67. Masters B, Kelley E, Quaife C and Brinster R (1994a) Targeted disruption of metallothionein I and II genes increases sensitivity to cadmium. Proc. Natl. Acad. Sci. USA 91, 584-588.
68. Masters B, Quaife C, Erickson J, et al (1994b) Metallothionein III is expressed in neurons that sequester zinc in synaptic vesicles. J. Neuroscience 14, 5844-5857.
69. Mercer J, Paynter J and Grimes A (1994) The toxic milk mouse does have elevated hepatic metallothionein mRNA. Biochem. J. 304, 317-318.
70. Michalska A and Choo K (1993) Targeting and germ-line transmission of a null mutation at the metallothionein I and II loci in mouse. Proc. Natl. Acad. Sci. USA 90, 8088-8092.
71. Min K-S, Terano Y, Onosaka S and Tanaka K (1991) Induction of hepatic metallothionein by non-metallic compounds associated with acute-phase response in inflammation. Toxicol. Appl. Pharmacol. 111, 152-162.
72. Min K-S, Mukai S, Ohta M, Onosaka S and Tanaka K (1992) Glucocorticoid inhibition of inflammation-induced metallothionein synthesis in mouse liver. Toxicol. Appl. Pharmacol. 113, 293-298.
73. Muller T, Schukelt R and Jaenicke L (1991) Cadmium/zinc-metallothionein induces DNA strand breaks in vitro. Arch. Toxicol. 65, 20-26.
74. Muller T, Schuckelt R and Jaenicke L (1994) Evidence for radical species as intermediates in cadmium/zinc-metallothionein-dependent DNA damage in vitro. Environ. Health Perspect. 102, 27-29.
75. Munro S and Pelham H (1986) An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell 46, 291-300.
76. Olafson R (1985) Thymus metallothionein: regulation of zinc-thionein in the aging mouse. Can. J. Biochem. Cell Biol. 63, 91-95.
77. Otsuka F, Iwamatsu A, Suzuki K, Ohsawa M, Hamer D and Koizumi S (1994) Purification and characterization of a protein that binds to metal responsive elements of the human metallothionein IIA gene. J. Biol. Chem. 269, 23700-23707.
78. Palmiter R (1987) Molecular biology of metallothionein gene expression. In: Metallothionein II. Experientia Supplementum, eds J Kagi and Y Kojima, Birkhauser Verlag, Basel, 63-80.
79. Palmiter R, Findley S, Whitmore T and Durnam D (1992) MT-III, a brain-specific member of the metallothionein gene family. Proc. Natl. Acad. Sci. USA 89, 6333-6337.
80. Parakh K and Kannan K (1993) Demonstration of a ubiquitin binding protein site on murine haemopoietic progenitor cells: implication of ubiquitin in homing and adhesion. Br. J. Haematol. 84, 212-219.
81. Pauwels M (1994) Induction by zinc of specific metallothionein isoforms in human monocytes. Eur. J. Biochem. 220, 105-110.
82. Pierce S, DeNagel D and VanBuskirle A (1991) A role for heat-shock proteins in antigen processing and presentation. Curr. Top. Microbiol. Immunol. 167, 83-92.
83. Plisov S, Merkulova T and Shkapenko A (1994a) Short glucocorticoid-responsive element in the 5′-flanking region of murine metallothionein I gene. Mol. Biol. 28, 274-277.
84. Plisov SY, Nichiporenko MG, Shkapenko AL, Kumarev VP, Baranova LV and Merkulova TI (1994b) The immediate vicinity of mouse metallothionein-I gene contains two sites conferring glucocorticoid inducibility to the heterologous promoter. FEBS Lett. 352, 339-341.
85. Quaife CJ, Findley SD, Erickson JC, Froelick GJ, Kelly EJ, Zambrowicz BP and Palmiter RD (1994) Induction of a new metallothionein isoform (MT-IV) occurs during differentiation of stratified squamous epithelia. Biochemistry 33, 7250-7259.
86. Radtke F, Heuchel R, Georgiev O, Hergersberg M, Gariglio M, Dembic Z and Shaffner W (1993) Cloned transcription factor MTF-1 activates the mouse metallothionein I promoter. EMBO J. 12, 1355-1362.
87. Riordan J and Jolicoeur-Paquet L (1982) Metallothionein accumulation may account for intracellular copper retention in Menkes' disease. J. Biol. Chem. 257, 4639-4645.
88. Robbins A, McRee D, Williamson M, et al (1991) Redefined crystal structure of Cd, Zn, metallothionein at 2.0 Å resolution. J. Mol. Biol. 221, 1269-1293.
89. Sargent C, Dunham I, Trowsdale J and Campell R (1989) Human major histocompatibility complex contains genes for the major heat-shock protein HSP70. Proc. Natl. Acad. Sci. USA 86, 1968-1972.
90. Sasagawa S, Matsubara J and Satow Y (1993) Stress-related induction of hepatic metallothionein synthesis and increase in peripheral polymorphonuclear leukocytes in mice. Immunopharmacol. Immunotoxicol. 15, 217-226.
91. Sato M and Bremner I (1993) Oxygen free radicals and metallothionein. Free Rad. Biol. Med. 14, 325-337.
92. Schmidt C, Jubier M and Hamer D (1985) Structure and expression of two human metallothionein-I isoform genes and a related pseudogene. J. Biol. Chem. 260, 7731-7737.
93. Searle PF (1987) Metallothionein gene regulation. Biochem. Soc. Transact. 15, 584-586.
94. Sewell A, Jensen L, Erickson J, Palmiter R and Winge D (1995) Bioactivity of metallothionein-3 correlates with its novel b domain sequence rather than metal binding properties. Biochemistry 34, 4740-4747.
95. Shapiro S and Cousins R (1980) Induction of rat liver metallothionein mRNA and its distribution between free and membrane-bound polyribosomes. Biochem. J. 190, 755-764.
96. Shinji H, Akagawa KS and Yoshida T (1994) LPS induces selective translocation of protein kinase C-b in LPS-responsive mouse macrophages, but not in LPS-nonresponsive mouse macrophages. J. Immunol. 153, 5760-5771.
97. Shiraishi N, Yamamoto H, Takeda Y, Kondoh S, Hayashi H, Hashimoto K and Aono K (1986) Increased metallothionein content in rat liver and kidney following X-irradiation. Toxicol. Appl. Pharmacol. 85, 128-134.
98. Shiraishi N, Hochadel J, Coogan T, Koropatnick J and Waalkes M (1995) Sensitivity to cadmium-induced genotoxicity in rat testicular cells is associated with minimal expression of the metallothionein gene. Toxicol. Appl. Pharmacol. 130, 229-236.
99. Shworak N, O'Connor T, Wong N and Gedamu L (1993) Distinct TATA motifs regulate differential expression of human metallothionein I genes MT-If and MT-Ig. J. Biol. Chem. 268, 24460-24466.
100. Smith H, Fried V and Weissman I (1986) Expression cloning of a lymphocyte homing receptor cDNA: ubiquitin is the reactive species. Science 231, 845-850.
101. Soumillion A, van Damme J and De Ley M (1992) Cloning and specific polymerised-chain-reaction amplification of a third charge-separable human metallothionein isoform. Eur. J. Biochem. 209, 999-1004.
102. Stennard FA, Holloway AF, Hamilton J and West AK (1994) Characterisation of six additional human metallothionein genes. Biochim. Biophys. Acta 1218, 357-365.
103. Stephenson G, Chan H and Cherian M (1994) Copper-metallothionein from the toxic milk mutant mouse enhances lipid peroxidation initiated by an organic hydroperoxide. Toxicol. Appl. Pharmacol. 125, 90-96.
104. Taplitz S, Calame K and Herschman H (1986) Alternative inducers of the rat metallothionein I gene cause distinct changes in chromatin structure in the 5′ region of the gene. Mol. Cell. Biol. 6, 2576-2581.
105. Thornalley P and Vasak M (1985) Possible roles for metallothionein in protection against radiation-induced oxidative stress. Kinetics and mechanism of its reaction with superoxide and hydroxyl radicals. Biochim. Biophys. Acta 827, 36-44.
106. Tsujikawa K, Suzuki N, Sagawa K, et al (1994) Induction and subcellular localization of metallothionein in regenerating rat liver. Eur. J. Cell Biol. 63, 240-246.
107. Udom A and Brady F (1980) Reactivation in vitro of zinc-requiring apo-enzymes by rat liver zinc-thionein. Biochem. J. 187, 329-335.
108. Udono H and Srivastava P (1993) Heat shock protein 70-associated peptides elicit specific cancer immunity. J. Exp. Med. 178, 1391-1396.
109. Waalkes M, Perantoni A and Rehm S (1989) Tissue susceptibility in cadmium carcinogenesis. Biol. Trace Elem. Res. 21, 483-490.
110. Wang X-P, Chan HM, Goyer RA and Cherian MG (1993) Nephrotoxicity of repeated injections of cadmium-metallothionein in rats. Toxicol. Appl. Pharmacol. 119, 11-16.
111. Webb M (1987) Metallothionein in regeneration, reproduction and development. In: Metallothionein II. Experiehtia Supplementum, eds J Kagi and Y Kojima, Birkhauser Verlag, Basel, 483-498.
112. Youn J, Borghesi L, Olson E and Lynes M (1995) Immunomodulatory effects of extracellular metallothionein II. Effects on macrophage functions. J. Toxicol. Env. Health 45, 397-413.
113. Zeng J, Heuchel R, Schaffner W and Kagi J (1991) Thionein (apometallothionein) can modulate DNA binding and transcription activation by zinc finger containing factor Sp1. FEBS Lett. 279, 310-312.