Metallothioneins are upregulated in symptomatic mice with astrocyte- targeted expression of tumor necrosis factor-α

Experimental Neurology

Volumn 163, Issue 1, 2000, Pages 46-54

  Carrasco, Javier ^a   Giralt, Mercedes ^a   Penkowa, Milena ^b   Stalder, Anna K ^c   Campbell, Iain L ^c   Hidalgo, Juan ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; METALLOTHIONEIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN INJURY; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; IMMUNOPATHOLOGY; LYMPHOCYTIC INFILTRATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION;

EID: 0034069770     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1999.7335     Document Type: Article

References (66)

1. Akwa Y., Hassett D. E., Eloranta M.-L., Sandberg K., Masliah E., Powell H., Whitton J. L., Bloom F. E., Campbell I. L. Transgenic expression of IFN-α in the central nervous system of mice protects against lethal neurotropic viral infection but induce inflammation and neurodegeneration. J. Immunol. 161:1998;5016-5026.
2. Amoureux M., Van Gool D., Herrero M., Dom R., Colpaert F., Pauwels P. Regulation of metallothionein-III (GIF) mRNA in the brain of patients with Alzheimer disease is not impaired. Mol. Chem. Neuropathol. 32:1997;101-121.
3. Aschner M. The functional significance of brain metallothioneins. FASEB J. 10:1996;1129-1136.
4. Aschner M., Cherian M. G., Klaassen C. D., Palmiter R. D., Erickson J. C., Bush A. I. Metallothioneins in brain - The role in physiology and pathology. Toxicol. Appl. Pharmacol. 142:1997;229-242.
5. Barnum S. R., Jones J. L., Müller-Ladner U., Samimi A., Campbell I. L. Chronic complement C3 gene expression in the CNS of transgenic mice with astrocyte-targeted interleukin-6 expression. Glia. 18:1996;107-117.
6. Brett F. M., Mizisin A. P., Powell H., Campbell I. L. Evolution of neuropathological abnormalities associated with blood-brain barrier breakdown in transgenic mice expressing interleukin-6 in astrocytes. J. Neuropathol. Exp. Neurol. 54:1995;766-775.
7. Campbell I. L. Transgenic mice and cytokine actions in the brain: Bridging the gap between structural and functional neuropathology. Brain Res. Rev. 26:1998;327-336.
8. Campbell I. L., Abraham C. R., Masliah E., Kemper P., Inglis J. D., Oldstone M. B. A., Mucke L. Neurologic disease in transgenic mice by cerebral overexpression of interleukin 6. Proc. Natl. Acad. Sci. USA. 90:1993;10061-10065.
9. Carrasco J., Giralt M., Molinero A., Penkowa M., Moos T., Hidalgo J. Metallothionein (MT)-III: Generation of polyclonal antibodies, comparison with MT-I + II in the freeze lesioned rat brain and in a bioassay with astrocytes, and analysis of Alzheimer's disease brains. J. Neurotrauma. 16:1999;1115-1129.
10. Carrasco J., Hernández J., Bluethmann H., Hidalgo J. Interleukin-6 and tumor necrosis factor-alpha type 1 receptor deficient mice reveal a role of IL-6 and TNF-alpha on brain metallothionein-I and -III regulation. Mol. Brain Res. 57:1998;221-234.
11. Carrasco J., Hernández J., González B., Campbell I. L., Hidalgo J. Localization of metallothionein-I and -III expression in the CNS of transgenic mice with astrocyte-targeted expression of interleukin 6. Exp. Neurol. 153:1998;184-194.
12. Castelnau P. A., Garrett R. S., Palinski W., Witztum J. L., Campbell I. L., Powell H. C. Abnormal iron deposition associated with lipid peroxidation in transgenic mice expressing interleukin-6 in the brain. J. Neuropathol. Exp. Neurol. 57:1998;268-282.
13. Chiang C.-S., Powell H. C., Gold L. H., Samimi A., Campbell I. L. Macropahe/microglial-mediated primary demyelination and motor disease induced by the central nervous system production of interleukin-3 in transgenic mice. J. Clin. Invest. 97:1996;1512-1524.
14. Chiang C.-S., Stalder A. K., Samimi A., Campbell I. L. Reactive gliosis as a consequence of interleukin 6 expression in the brain: studies in transgenic mice. Dev. Neurosci. 16:1994;212-221.
15. Coyle P., Philcox J. C., Rofe A. M. Metallothionein induction in freshly isolated rat hepatocytes. Biol. Trace Elem. Res. 36:1993;35-49.
16. Coyle P., Philcox J. C., Rofe A. M. Metallothionein induction in cultured rat hepatocytes by arthritic rat serum, activated macrophages, interleukin-6, interleukin-11 and leukaemia inhibitory factor. Inflamm. Res. 44:1995;475-481.
17. Dalton T. P., Palmiter R. D., Andrews G. K. Transcriptional induction of the mouse metallothionein-I gene in hydrogen peroxide-treated Hepa cells involves a composite major late transcription factor/antioxidant response element and metal response promoter elements. Nucleic Acids Res. 22:1994;5016-5023.
18. Dalton T. P., Li Q., Bittel D., Liang L., Andrews G. K. Oxidative stress activates metal-responsive transcription factor-1 binding activity. Occupancy in vivo of metal response elements in the metallothionein-I gene promoter. J. Biol. Chem. 271:1996;26233-26241.
19. De S. K., McMaster M. T., Andrews G. K. Endotoxin induction of murine metallothionein gene expression. J. Biol. Chem. 265:1990;15267-15274.
20. Erickson J. C., Hollopeter G., Thomas S. A., Froelick G. J., Palmiter R. D. Disruption of the metallothionein-III gene in mice: Analysis of brain zinc, behavior, and neuron vulnerability to metals, aging, and seizures. J. Neurosci. 17:1997;1271-1281.
21. Erickson J. C., Sewell A. K., Jensen L. T., Winge D. R., Palmiter R. D. Enhanced neurotrophic activity in Alzheimer's disease cortex is not associated with down-regulation of metallothionein-III (GIF). Brain Res. 649:1994;297-304.
22. Fu K., Tomita T., Sarras M., De Lisle R., Andrews G. K. Metallothionein protects against cerulein-induced acute pancreatitis: Analysis using transgenic mice. Pancreas. 17:1998;238-246.
23. Gasull T., Giralt M., Hernandez J., Martinez P., Bremner I., Hidalgo J. Regulation of metallothionein concentrations in rat brain: Effect of glucocorticoids, zinc, copper, and endotoxin. Am. J. Physiol. 266:1994;E760-E767.
24. Gasull T., Rebollo D. V., Romero B., Hidalgo J. Development of a competitive double antibody radioimmunoassay for rat metallothionein. J. Immunoassay. 14:1993;209-225.
25. Ghirnikar R. S., Lee Y. L., Eng L. F. Inflammation in traumatic brain injury: Roles of cytokines and chemokines. Neurochem. Res. 23:1998;329-340.
26. Grimble R., Bremner I. Tumor necrosis factor α enhances hepatic metallothionein-I content but reduces that of the kidney. Proc. Nutr. Soc. 48:1989.
27. Halliwell B. Reactive oxygen species and the central nervous system. J. Neurochem. 59:1992;1609-1623.
28. Hanada K., Sawamura D., Tamai K., Baba T., Hashimoto I., Muramatsu T., Miura N., Naganuma A. Novel function of metallothionein in photoprotection: metallothionein-null mouse exhibits reduced tolerance against ultraviolet B injury in the skin. J. Invest. Dermatol. 111:1998;582-585.
29. Hernández J., Giralt M., Belloso E., Rebollo D. V., Romero B., Hidalgo J. Interactions between metallothionein inducers in rat liver and primary cultures of rat hepatocytes. Chem. Biol. Interact. 100:1996;27-40.
30. Hernández J., Molinero A., Campbell I. L., Hidalgo J. Transgenic expression of interleukin 6 in the central nervous system regulates brain metallothionein-I and -III expression in mice. Mol. Brain Res. 48:1997;125-131.
31. Heyser C. J., Masliah E., Samimi A., Campbell I. L., Gold L. H. Progressive decline in avoidance learning paralleled by inflammatory neurodegeneration in transgenic mice expressing interleukin 6 in the brain. Proc. Natl. Acad. Sci. USA. 94:1997;1500-1505.
32. Hidalgo J., Campmany L., Borras M., Garvey J. S., Armario A. Metallothionein response to stress in rats: Role in free radical scavenging. Am. J. Physiol. 255:1988;E518-E524.
33. Hidalgo J., Castellano B., Campbell I. L. Regulation of brain metallothioneins. Curr. Topics Neurochem. 1:1997;1-26.
34. Hoey J. G., Garrett S. H., Sens M. A., Todd J. H., Sens D. A. Expression of MT-3 mRNA in human kidney, proximal tubule cell cultures, and renal cell carcinoma. Toxicol. Lett. 92:1997;149-160.
35. Hopkins S. J., Rothwell N. J. Cytokines and the nervous system. I: Expression and recognition. Trends Neurosci. 18:1995;83-88.
36. Hozumi I., Inuzuka T., Tsuji S. Brain injury and growth inhibitory factor (GIF) - A minireview. Neurochem. Res. 23:1998;319-328.
37. Kang Y. J., Chen Y., Yu A. D., Voss-McCowan M., Epstein P. N. Overexpression of metallothionein in the heart of transgenic mice suppresses doxorubicin cardiotoxicity. J. Clin. Invest. 100:1997;1501-1506.
38. Knoblach S. M., Faden A. I. Interleukin-10 improves outcome and alters proinflammatory cytokine expression after experimental traumatic brain injury. Exp. Neurol. 153:1998;143-151.
39. Kondo Y., Rusnak J., Hoyt D., Settineri C., Pitt B. R., Lazo J. S. Enhanced apoptosis in metallothionein null cells. Mol. Pharmacol. 52:1997;195-201.
40. Lazo J. S., Kondo Y., Dellapiazza D., Michalska A. E., Choo K. H., Pitt B. R. Enhanced sensitivity to oxidative stress in cultured embryonic cells from transgenic mice deficient in metallothionein I and II genes. J. Biol. Chem. 270:1995;5506-5510.
41. Liang L., Fu K., Lee D. K., Sobieski R. J., Dalton T., Andrews G. K. Activation of the complete mouse metallothionein gene locus in the maternal deciduum. Mol. Reprod. Dev. 43:1996;25-37.
42. Liu J., Liu Y., Habeebu S., Klaassen C. D. Metallothionein (MT)-null mice are sensitive to cisplatin-induced hepatotoxicity. Toxicol. Appl. Pharmacol. 149:1998;24-31.
43. Liu J., Liu Y., Hartley D., Klaassen C. D., Shehin-Johnson S. E., Lucas A., Cohen S. D. Metallothionein-I/II knockout mice are sensitive to acetaminophen-induced hepatotoxicity. J. Pharmacol. Exp. Ther. 289:1999;580-586.
44. Liu J., Liu Y. P., Sendelbach L. E., Klaassen C. D. Endotoxin induction of hepatic metallothionein is mediated through cytokines. Toxicol. Appl. Pharmacol. 109:1991;235-240.
45. Martiney J. A., Cuff C., Litwak M., Berman J., Brosnan C. F. Cytokine-induced inflammation in the central nervous system revisited. Neurochem. Res. 23:1998;349-359.
46. McIntosh T. K., Juhler M., Wieloch T. Novel pharmacologic strategies in the treatment of experimental traumatic brain injury. J. Neurotrauma. 15:1998;731-769.
47. Moffatt P., Séguin C. Expression of the gene encoding metallothionein-3 in organs of the reproductive system. DNA Cell. Biol. 17:1998;501-510.
48. Palmiter R. D., Findley S. D., Whitmore T. E., Durnam D. M. MT-III, a brain-specific member of the metallothionein gene family. Proc. Natl. Acad. Sci. USA. 89:1992;6333-6337.
49. Penkowa M., Carrasco J., Giralt M., Moos T., Hidalgo J. CNS wound healing is severely depressed in metallothionein-I + II deficient mice. J. Neurosci. 19:1999;2535-2545.
50. Penkowa M., Giralt M., Moos T., Thomsen P., Hernández J., Hidalgo J. Impaired inflammatory response to glial cell death in genetically metallothionein-I and -II deficient mice. Exp. Neurol. 156:1999;149-164.
51. Penkowa M., Moos T., Carrasco J., Hadberg H., Molinero A., Bluethmann H., Hidalgo J. Strongly compromised inflammatory response to brain injury in interleukin-6 deficient mice. Glia. 25:1999;343-357.
52. Powell H. C., Campbell I. L. Ultrastructural abnormalities of glia and blood-brain barrier in a transgenic mouse overexpressing interleukin-6. Brain Pathol. 4:1994;278-279.
53. Quaife C. J., Findley S. D., Erickson J. C., Froelick G. J., Kelly E. J., Zambrowicz B. P., Palmiter R. D. Induction of a new metallothionein isoform (MT-IV) occurs during differentiation of stratified squamous epithelia. Biochemistry. 33:1994;7250-7259.
54. Rothwell N. J., Hopkins S. J. Cytokines and the nervous system II: Actions and mechanisms of action. Trends Neurol. Sci. 18:1995;130-136.
55. Sato M., Bremner I. Oxygen free radicals and metallothionein. Free Radic. Biol. Med. 14:1993;325-337.
56. Sato M., Sasaki M., Hojo H. Tissue specific induction of metallothionein synthesis by tumor necrosis factor-alpha. Res. Commun. Chem. Pathol. Pharmacol. 75:1992;159-172.
57. Sato M., Sasaki M., Hojo H. Differential induction of metallothionein synthesis by interleukin-6 and tumor necrosis factor-alpha in rat tissues. Int. J. Immunopharmacol. 16:1994;187-195.
58. Sato M., Sasaki M., Hojo H. Antioxidative roles of metallothionein and manganese superoxide dismutase induced by tumor necrosis factor-alpha and interleukin-6. Arch. Biochem. Biophys. 316:1995;738-744.
59. Stalder A. K., Carson M. J., Pagenstecher A., Asensio V. C., Kincaid C., Benedict M., Powell H. C., Masliah E., Campbell I. L. Late-onset chronic inflammatory encephalopathy in immune-competent and severe combined immune-deficient (SCID) mice with astrocyte-targeted expression of tumor necrosis factor. Am. J. Pathol. 153:1998;767-783.
60. Steffensen S. C., Campbell I. L., Henriksen S. J. Site-specific hippocampal pathophysiology due to cerebral overexpression of interleukin-6 in transgenic mice. Brain Res. 652:1994;149-153.
61. Stichel C., Verner Müller H. Experimental strategies to promote axonal regeneration after traumatic central nervous system injury. Progr. Neurobiol. 56:1998;119-148.
62. Taubeneck M. W., Daston G. P., Rogers J. M., Gershwin M. E., Ansari A., Keen C. L. Tumor necrosis factor-alpha alters maternal and embryonic zinc metabolism and is developmentally toxic in mice. J. Nutr. 125:1995;908-919.
63. Thornalley P. J., Vasak M. Possible role for metallothionein in protection against radiation-induced oxidative stress. Kinetics and mechanism of its reaction with superoxide and hydroxyl radicals. Biochim. Biophys. Acta. 827:1985;36-44.
64. Uchida Y., Takio K., Titani K., Ihara Y., Tomonaga M. The growth inhibitory factor that is deficient in the Alzheimer's disease brain is a 68 amino acid metallothionein-like protein. Neuron. 7:1991;337-347.
65. Unsicker K., Grothe C., Westermann R., Wewetzer K. Cytokines in neural regeneration. Curr. Opin. Neurobiol. 2:1992;671-678.
66. Yagle M. K., Palmiter R. D. Coordinate regulation of mouse metallothionein I and II genes by heavy metals and glucocorticoids. Mol. Cell. Biol. 5:1985;291-294.