Transgenic expression of interleukin 6 in the central nervous system regulates brain metallothionein-I and -III expression in mice

Molecular Brain Research

Volumn 48, Issue 1, 1997, Pages 125-131

  Hernández, Joaquín ^a   Molinero, A ^a   Campbell, Iain L ^b   Hidalgo, Juan ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Brain; Endotoxin; Growth inhibitory factor; IL 6; Liver; Metallothionein I; Metallothionein II; Metallothionein III

Indexed keywords

ACUTE PHASE PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 6; ISOPROTEIN; MESSENGER RNA; METALLOTHIONEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CONTROLLED STUDY; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HYPOTHALAMUS; MEDULLA OBLONGATA; MOUSE; NERVE DEGENERATION; NONHUMAN; PONS; PRIORITY JOURNAL; PROMOTER REGION; RECOMBINANT GENE; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; BRAIN; CELLS, CULTURED; EMBRYO; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN-1; METALLOTHIONEIN; MICE; MICE, TRANSGENIC; MULTIGENE FAMILY; NEURONS; ORGAN SPECIFICITY; PROMOTER REGIONS (GENETICS); PROTEIN BIOSYNTHESIS; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

ANIMALIA; MUS MUSCULUS;

EID: 17044453671     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-328X(97)00087-9     Document Type: Article

References (49)

1. Akika S., Hirano T., Taga T., Kishimoto T. Biology of multifunctional cytokines: IL 6 and related molecules (IL 1 and TNF). FASEB J. 5:1990;2860-2867.
2. Anezaki T., Ishiguro H., Hozumi I., Inuzuka T., Hiraiwa M., Kobayashi H., Yuguchi T., Wanaka A., Uda Y., Miyatake T., Yamada K., Tohyama M., Tsuji S. Expression of growth inhibitory factor (GIF) in normal and injured rat brains. Neurochem. Int. 27:1995;89-94.
3. Badley J.E., Bishop G.A., St. John T., Frelinger J.A. A simple rapid method for the purification of poly A+ RNA. Biotechniques. 6:1988;114-119.
4. Barnum, S.R., Jones, J.L., Müller-Ladner, U., Samimi, A. and Campbell, I., Chronic complement C3 gene expression in the CNS of transgenic mice with astrocyte-targeted interleukin-6 expression, Glia, in press.
5. Bauer J., Ganter U., Abel J., Strauss S., Jonas U., Weib R., Gebicke-Haerter P., Volk B., Berger M. Effects of interleukin-1 and interleukin-6 on metallothionein and amyloid precursor protein expression in human neuroblastoma cells. Evidence that interleukin-6 possibly acts via a receptor different from the 80-kDa interleukin-6 receptor. J. Neuroimmunol. 45:1993;163-174.
6. 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.
7. Chiang C.-S., Stalder A., 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.
8. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
9. Cousins R.J., Leinart A.S. Tissue-specific regulation of zinc metabolism and metallothionein genes by interleukin-1. FASEB J. 2:1988;2884-2890.
10. Dalton T., Pazdernik T.L., Wagner J., Samson F., Andrews G.K. Temporalspatial patterns of expression of metallothionein-I and -III and other stress related genes in rat brain after kainic acid-induced seizures. Neurochem. Int. 27:1995;59-71.
11. De S.K., McMaster M.T., Andrews G.K. Endotoxin induction of murine metallothionein gene expression. J. Biol. Chem. 265:1990;15267-15274.
12. Duguid J.R., Bohmont C.W., Liu N., Tourtellotte W.W. Changes in brain gene expression shared by scrapie and Alzheimer disease. Proc. Natl. Acad. Sci. USA. 86:1989;7260-7264.
13. Gasull T., Giralt M., García A., Hidalgo J. Regulation of metallothionein-I+II levels in specific brain areas and liver in the rat: role of catecholamines. Glia. 12:1994;135-143.
14. Gasull T., Giralt M., Hernández J., Martínez 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.
15. 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.
16. Heinrich P., Castell J.V., Andus T. Interleukin-6 and the acute phase response. Biochem. J. 265:1990;621-636.
17. Hidalgo J., Borrás M., Garvey J.S, Armario A. Liver, brain, and heart metallothionein induction by stress. J. Neurochem. 55:1990;651-654.
18. Hidalgo J., Campmany L., Borrás M., Garvey J.S., Armario A. Metallothionein response to stress: role in free radical scavenging. Am. J. Physiol. 255:1988;E518-E524.
19. Hidalgo J., Campmany L., Martí O., Armario A. Metallothionein-I induction by stress in specific brain areas. Neurochem. Res. 16:1991;1145-1148.
20. Hidalgo J., García A., Oliva A.M., Giralt M., Gasull T., González B., Milnerowicz H., Wood A., Bremner I. Effect of zinc, copper and glucocorticoids on metallothionein levels of cultured neurons and astrocytes from rat brain. Chem. Biol. Interact. 93:1994;197-219.
21. Hidalgo J., Gasull T., Giralt M., Armario A. Brain metallothionein in stress. Biol. Signals. 3:1994;198-210.
22. Hozumi I., Inuzuka T., Hiraiwa M., Uchida Y., Anezaki T., Ishiguro H., Kobayashi H., Uda Y., Miyatake T., Tsuji S. Changes of growth inhibitory factor after stab wounds in rat brain. Brain Res. 688:1995;143-148.
23. Imagawa M., Ishikawa Y., Shimano H., Osada S., Nishihara T. CTG triplet repeat in mouse growth inhibitory factor/metallothionein III gene promoter represses the transcriptional activity of the heterologous promoters. J. Biol. Chem. 270:1995;20898-20900.
24. Inglis J.D., Lee M., Davidson D.R., Hill R.E. Isolation of two cDNAs encoding novel a1-antichymotrypsin-like proteins in a murine chondrocytic cell line. Gene. 106:1991;213-222.
25. Kägi, J.H.R. and Kojima, Y. (Eds.), Metallothionein II, Birkhäuser, Basel, Switzerland, 1987.
26. Kikuchi Y., Irie M., Kasahara T., Sawada J.-I., Terao T. Induction of metallothionein in a human astrocytoma cell line by interleukin-1 and heavy metals. FEBS Lett. 317:1993;22-26.
27. Kramer K.K., Liu J., Choudhuri S., Klaassen C.D. Induction of metallothionein mRNA and protein in murine astrocyte cultures. Toxicol. Appl. Pharmacol. 136:1996;94-100.
28. Lazo J.S., Kondo Y., Dellapiazza D., Michalska A.E., Andy 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.
29. Lehman-McKeeman, L.D., Kershaw, W.C. and Klaassen, C.D., Species differences in metallothionein regulation: a comparison of the induction of isometallothioneins in rats and mice. In C.D. Klaassen and K.T. Suzuki (Eds.), Metallothionein in Biology and Medicine, CRC, 1991, pp. 121-131.
30. Löffner F., Lohmann S.M., Walckhoff B., Walter V., Hamprecht H.B. Immunocytochemical characterization of neuron-enriched primary cultures of embryonic rat brain cells by established neuronal and glial markers by monospecific antisera against cyclic nucleotide-dependent protein quinases and the synaptic vesicle protein synapsin-I. Brain. Res. 363:1986;205-221.
31. Masters B.A., Quaife C.J., Erickson J.C., Kelly E.J., Froelick G.J., Zambrowicz B.P., Brinster R.L., Palmiter R.D. Metallothionein III is expressed in neurons that sequester zinc in synaptic vesicles. J. Neurosci. 14:1994;5844-5857.
32. Merrill J.E., Jonakait G.M. Interactions of the nervous and immune systems in development, normal brain homeostasis, and disease. FASEB J. 9:1995;611-618.
33. Muramami N., Fukata J., Tsukada T., Kobayashi H., Ebisui O., Segawa H., Muro S., Imura H., Nakao K. Bacterial lipopolysaccharide-induced expression of interleukin-6 messenger ribonucleic acid in the rat hypothalamus, pituitary, adrenal gland, and spleen. Endocrinology. 133:1993;2574-2578.
34. Naruse S., Igarashi S.-i., Furuya T., Kobayashi H., Miyatake T., Tsuji S. Structures of the human and mouse growth inhibitory factor-encoding genes. Gene. 144:1994;283-287.
35. Paliwall V.K., Iversen P.L., Ebadi M. Regulation of zinc metallothionein II mRNA level in rat brain. Neurochem. Int. 17:1990;441-447.
36. Palmiter R.D., Findley S.D., Whitmore T.E., Durnam D. MT-III, a brain-specific member of the metallothionein gene family. Proc. Natl. Acad. Sci. USA. 89:1992;6333-6337.
37. Penkowa M., Moos T. Disruption of the blood-interface in neonatal rat neocortex induces a transient expression of metallothionein in reactive astrocytes. Glia. 13:1995;217-227.
38. 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.
39. Sambrook, J., Fritsch, E.F. and Maniatis, T., Molecular Cloning, 2nd edn., Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, 1989.
40. Sato M., Bremner I. Oxygen free radicals and metallothionein. Free Rad. Biol. Med. 14:1993;325-337.
41. Schroeder J.J., Cousins R.J. Interleukin 6 regulates metallothionein gene expression and zinc metabolism in hepatocyte monolayer cultures. Proc. Natl. Acad. Sci. USA. 87:1990;3137-3141.
42. Sillevis Smitt P.A.E., Mulder T.P.J., Verspaget H.W., Blaauwgeers H.G.T., Troost D., Vianney de Jong J.M.B. Metallothionein in amytrophic lateral sclerosis. Biol. Signals. 3:1994;193-197.
43. Suzuki, K.T., Imura, N. and Kimura, M. (Eds.), Metallothionein III, Birkhäuser, Basel, Switzerland, 1993.
44. 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.
45. 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.
46. Vasconcelos M.H., Tam S.-C., Beattie J.H., Hesketh J.E. Evidence for differences in the post-transcriptional regulation of rat metallothionein isoforms. Biochem. J. 315:1996;665-671.
47. Yuguchi T., Kohmura E., Yamada K., Sakaki T., Yamashita T., Otsuki H., Wanaka A., Tohyama M., Tsuji S., Hayakawa T. Changes in growth inhibitory factor mRNA expression compared with those in c-jun mRNA expression following facial nerve transection. Mol. Brain Res. 28:1995;181-185.
48. Yuguchi T., Kohmura E., Yamada K., Sakaki T., Yamashita T., Otsuki H., Kataoka K., Tsuji S., Hayakawa T. Expression of growth inhibitory factor mRNA following cortical injury in rat. J. Neurotrauma. 12:1995;299-306.
49. Zheng H., Berman N.E.J., Klaassen C.D. Chemical modulation of metallothionein I and III mRNA in mouse brain. Neurochem. Int. 27:1995;43-58.