Ultrastructural study of depolarization-induced translocation of NRF-2 transcription factor in cultured rat visual cortical neurons

European Journal of Neuroscience

Volumn 19, Issue 5, 2004, Pages 1153-1162

  Yang, Shou Jing ^a   Liang, Huan Ling ^a   Ning, Gang ^a   Wong Riley, Margaret T T ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Cytochrome oxidase; Electron microscopy; Immunogold silver staining; Nuclear respiratory factor 2

Indexed keywords

CELL DNA; GA BINDING PROTEIN; NUCLEAR RESPIRATORY FACTOR 2ALPHA; NUCLEAR RESPIRATORY FACTOR 2BETA; POTASSIUM CHLORIDE; PROTEIN SUBUNIT; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIBODY SPECIFICITY; ARTICLE; CELL ACTIVITY; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; DEPOLARIZATION; GENETIC TRANSCRIPTION; GOLGI COMPLEX; HETEROCHROMATIN; IMMUNOGOLD LABELING; NERVE CELL; NERVE CELL CULTURE; NEWBORN; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RAT; RIBOSOME; SILVER STAINING; TRANSACTIVATION; TRANSCRIPTION INITIATION; VISUAL CORTEX;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANIMALS, NEWBORN; CELL NUCLEUS; CELLS, CULTURED; CYTOPLASM; DNA-BINDING PROTEINS; GA-BINDING PROTEIN TRANSCRIPTION FACTOR; MEMBRANE POTENTIALS; NEURONS; POTASSIUM CHLORIDE; RATS; TRANSCRIPTION FACTORS; VISUAL CORTEX;

EID: 1642267301     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2004.03250.x     Document Type: Article

References (55)

1. Aoki, K., Meng, G., Suzuki, K., Takashi, T., Kameoka, Y., Nakahara, K., Ishida, R. & Kasai, M. (1998) RP58 associates with condensed chromatin and mediates a sequence-specific transcriptional repression. J. Biol. Chem., 273, 26698-26704.
2. Balazs, R., Resink, A., Hack, N., Van der Valk, J.B., Kumar, K.N. & Michaelis, E. (1992) NMDA treatment and K(+)-induced depolarization selectively promote the expression of an NMDA-preferring class of the ionotropic glutamate receptors in cerebellar granule neurones. Neurosci. Lett., 137, 109-113.
3. Basu, A., Park, K., Atchison, M.L., Carter, R.S. & Avadhani, N.G. (1993) Identification of a transcriptional initiator element in the cytochrome c oxidase subunit Vb promoter which binds to transcription factors NF-E1 (YY-1, delta) and Spl. J. Biol. Chem., 268, 4188-4196.
4. Baughman, R.W., Huettner, J.E., Jones, K.A. & Khan, A.A. (1991) Cell culture of neocortex and basal forebrain from postnatal rats. In Banker, G. & Goslin, K. (Eds), Culturing Nerve Cells. The MIT Press, Cambridge, MA, pp. 227-249.
5. Bottenstein, J.E. (1985) Growth and differentiation of neural cells in defined media. In Bottenstein, J.E. & Sato, G. (Eds), Cell Cultures in the Neuroscience. Plenum Press, New York, pp. 3-44.
6. Boulukos, K.E., Pognonec, P., Rabault, B., Begue, A. & Ghysdael, J. (1989) Definition of an Ets 1 protein domain required for nuclear localization in cells and DNA-binding activity in vitro. Mol. Cell Biol., 9, 5718-5721.
7. Briguet, A. & Ruegg, M.A. (2000) The Ets transcription factor GABP is required for postsynaptic differentiation in vivo. J. Neurosci., 20, 5989-5996.
8. Carter, R.S. & Avadhani, N.G. (1994) Cooperative binding of GA-binding protein transcription factors to duplicated transcription initiation region repeats of the cytochrome c oxidase subunit IV gene. J. Biol. Chem., 269, 4381-4387.
9. Carter, R.S., Bhat, N.K., Basu, A. & Avadhani, N.G. (1992) The basal promoter elements of murine cytochrome c oxidase subunit IV gene consist of tandemly duplicated ets motifs that bind to GABP-related transcription factors. J. Biol. Chem., 267, 23418-23426.
10. Chinenov, Y., Schmidt, T., Yang, X.Y. & Martin, M.E. (1998) Identification of redox-sensitive cysteines in GA-binding protein-alpha that regulate DNA binding and heterodimerization. J. Biol. Chem., 273, 6203-6209.
11. Clarke, D.D. & Sokoloff, L. (1994) Circulation and energy metabolism of the brain. In Siegel, G.J., Agranoff, B.W., Albers, R.W. & Morinoff, P.B. (Eds), Basic Neurochemistry. Raven Press, New York, pp. 645-680.
12. Dong, X., Ghoshal, K., Majumder, S., Yadav, S.P. & Jacob, S.T. (2002) Mitochondrial transcription factor A and its downstream targets are upregulated in a rat hepatoma. J. Biol. Chem., 277, 43309-43318.
13. Erecinska, M. & Silver, I.A. (1989) ATP and brain function. J. Cereb. Blood Flow Metab., 9, 2-19.
14. Fisher, R.P. & Clayton, D.A. (1985) A transcription factor required for promoter recognition by human mitochondrial RNA polymerase. Accurate initiation at the heavy-and light-strand promoters dissected and reconstituted in vitro. J. Biol. Chem., 260, 11330-11338.
15. Flory, E., Hoffmeyer, A., Smola, U., Rapp, U.R. & Bruder, J.T. (1996) Raf-1 kinase targets GA-binding protein in transcriptional regulation of the human immunodeficiency virus type 1 promoter. J. Virol., 70, 2260-2268.
16. Frenster, J.H. (1972) Ultrastructural probes of chromatin within living human lymphocytes. Nat. New Biol., 236, 175-176.
17. Fromm, L. & Burden, S.J. (1998) Synapse-specific and neuregulin-induced transcription require an ets site that binds GABPalpha/GABPbeta. Genes Dev., 12, 3074-3083.
18. Fromm, L. & Burden, S.J. (2001) Neuregulin-1-stimulated phosphorylation of GABP in skeletal muscle cells. Biochemistry, 40, 5306-5312.
19. Goslin, K. & Banker, G. (1991) Rat hippocampal neurons in low-density culture. In Banker, G. & Goslin, K. (Eds), Culturing Nerve Cells. The MIT Press, Cambridge, MA, pp. 251-281.
20. Gugneja, S., Virbasius, J.V. & Scarpulla, R.C. (1995) Four structurally distinct, non-DNA-binding subunits of human nuclear respiratory factor 2 share a conserved transcriptional activation domain. Mol. Cell Biol., 15, 102-111.
21. Guo, A., Nie, F. & Wong-Riley, M. (2000) Human nuclear respiratory factor 2 alpha subunit cDNA: isolation, subcloning, sequencing, and in situ hybridization of transcripts in normal and monocularly deprived macaque visual system. J. Comp. Neurol., 417, 221-232.
22. Herdegen, T., Sandkuhler, J., Gass, P., Kiessling, M., Bravo, R. & Zimmermann, M. (1993) JUN, FOS, KROX, and CREB transcription factor proteins in the rat cortex: basal expression and induction by spreading depression and epileptic seizures. J. Comp. Neurol., 333, 271-288.
23. Hevner, R.F. & Wong-Riley, M.T. (1990) Regulation of cytochrome oxidase protein levels by functional activity in the macaque monkey visual system. J. Neurosci., 10, 1331-1340.
24. Hevner, R.F. & Wong-Riley, M.T. (1991) Neuronal expression of nuclear and mitochondrial genes for cytochrome oxidase (CO) subunits analyzed by in situ hybridization: comparison with CO activity and protein. J. Neurosci., 11, 1942-1958.
25. Hoffmeyer, A., Avots, A., Flory, E., Weber, C.K., Serfling, E. & Rapp, U.R. (1998) The GABP-responsive element of the interleukin-2 enhancer is regulated by JNK/SAPK-activating pathways in T lymphocytes. J. Biol. Chem., 273, 10112-10119.
26. Hughes, P.E., Alexi, T., Walton, M., Williams, C.E., Dragunow, M., Clark, R.G. & Gluckman, P.D. (1999) Activity and injury-dependent expression of inducible transcription factors, growth factors and apoptosis-related genes within the central nervous system. Prog. Neurobiol., 57, 421-450.
27. Janknecht, R. (1996) Analysis of the ERK-stimulated ETS transcription factor ER81. Mol. Cell Biol., 16, 1550-1556.
28. Kaur, R., Dikshit, K.L. & Raje, M. (2002) Optimization of immunogold labeling TEM: an ELISA-based method for evaluation of blocking agents for quantitative detection of antigen. J. Histochem. Cytochem., 50, 863-873.
29. Kuhn-Nentwig, L. & Kadenbach, B. (1985) Isolation and properties of cytochrome c oxidase from rat liver and quantification of immunological differences between isozymes from various rat tissues with subunit-specific antisera. Eur. J. Biochem., 149, 147-158.
30. LaMarco, K., Thompson, C.C., Byers, B.P., Walton, E.M. & McKnight, S.L. (1991) Identification of Ets- and notch-related subunits in GA binding protein. Science, 253, 789-792.
31. Larsson, N.G., Wang, J., Wilhelmsson, H., Oldfors, A., Rustin, P., Lewandoski, M., Barsh, G.S. & Clayton, D.A. (1998) Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat. Genet., 18, 231-236.
32. Lowry, O.H. (1975) Energy metabolism in brain and its control. In Ingvar, D.H. & Lassen, N.A. (Eds), Brain Work: the Coupling of Function, Metabolism, and Blood Flow in the Brain, Alfred Benzon Symposium VIII. Academic Press, New York, pp. 48-64.
33. Mao, S. & Medeiros, D.M. (2001) Nuclear respiratory factors 1 and 2 are upregulated in hearts from copper-deficient rats. Biol. Trace Elem. Res., 83, 57-68.
34. Martin, M.E., Chinenov, Y., Yu, M., Schmidt, T.K. & Yang, X.Y. (1996) Redox regulation of GA-binding protein-alpha DNA binding activity. J. Biol. Chem., 271, 25617-25623.
35. Mata, M., Fink, D.J., Gainer, H., Smith, C.B., Davidsen, L., Savaki, H., Schwartz, W.J. & Sokoloff, L. (1980) Activity-dependent energy metabolism in rat posterior pituitary primarily reflects sodium pump activity. J. Neurochem., 34, 213-215.
36. Nakatsu, S.L., Masek, M.A., Landrum, S. & Frenster, J.H. (1974) Activity of DNA templates during cell division and cell differentiation. Nature, 248, 334-335.
37. Nie, F. & Wong-Riley, M. (1999) Nuclear respiratory factor-2 subunit protein: correlation with cytochrome oxydase and regulation by functional activity in the monkey primary visual cortex. J. Comp. Neurol., 404, 310-320.
38. Oorschot, V., de Wit, H., Annaert, W.G. & Klumperman, J. (2002) A novel flat-embedding method to prepare ultrathin cryosections from cultured cells in their in situ orientation. J. Histochem. Cytochem., 50, 1067-1080.
39. Rodriguez-Pena, A., Escriva, H., Handler, A.C. & Vallejo, C.G. (2002) Thyroid hormone increases transcription of GA-binding protein/nuclear respiratory factor-2 alpha-subunit in rat liver. FEBS Lett., 514, 309-314.
40. Sawa, C., Goto, M., Suzuki, F., Watanabe, H., Sawada, J. & Handa, H. (1996) Functional domains of transcription factor hGABP beta1/E4TF1-53 required for nuclear localization and transcription activation. Nucl. Acids Res., 24, 4954-4961.
41. Scarpulla, R.C. (1997) Nuclear control of respiratory chain expression in mammalian cells. J. Bioenerg. Biomembr., 29, 109-119.
42. Scarpulla, R.C. (2002) Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochim. Biophys. Acta, 1576, 1-14.
43. Shinohara, M., Dollinger, B., Brown, G., Rapoport, S. & Sokoloff, L. (1979) Cerebral glucose utilization: local changes during and after recovery from spreading cortical depression. Science, 203, 188-190.
44. Somjen, G.G. (1979) Extracellular potassium in the mammalian central nervous system. Annu. Rev. Physiol., 41, 159-177.
45. Stevenson, A.S., Cartin, L., Wellman, T.L., Dick, M.H., Nelson, M.T. & Lounsbury, K.M. (2001) Membrane depolarization mediates phosphorylation and nuclear translocation of CREB in vascular smooth muscle cells. Exp. Cell Res., 263, 118-130.
46. Thompson, C.C., Brown, T.A. & McKnight, S.L. (1991) Convergence of Ets- and notch-related structural motifs in a heteromeric DNA binding complex. Science, 253, 762-768.
47. Villena, J.A., Vinas, O., Mampel, T., Iglesias, R., Giralt, M. & Villarroya, F. (1998) Regulation of mitochondrial biogenesis in brown adipose tissue: nuclear respiratory factor-2/GA-binding protein is responsible for the transcriptional regulation of the gene for the mitochondrial ATP synthase beta subunit. Biochem. J., 331, 121-127.
48. Virbasius, J.V. & Scarpulla, R.C. (1991) Transcriptional activation through ETS domain binding sites in the cytochrome c oxidase subunit IV gene. Mol. Cell Biol., 11, 5631-5638.
49. Virbasius, J.V. & Scarpulla, R.C. (1994) Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proc. Natl Acad. Sci. USA, 91, 1309-1313.
50. Virbasius, J.V., Virbasius, C.A. & Scarpulla, R.C. (1993) Identity of GABP with NRF-2, a multisubunit activator of cytochrome oxidase expression, reveals a cellular role for an ETS domain activator of viral promoters. Genes Dev., 7, 380-392.
51. Wong-Riley, M.T. (1989) Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci., 12, 94-101.
52. Wong-Riley, M., Guo, A., Bachman, N.J. & Lomax, M.I. (2000) Human COX6A1 gene: promoter analysis, cDNA isolation and expression in the monkey brain. Gene, 247, 63-75.
53. Wong-Riley, M.T.T., Nie, F., Hevner, R.F. & Liu, S. (1998) Brain cytochrome oxidase: functional significance and bigenomic regulation in the CNS. In Gonzalez-Lima, F. (Ed.), Cytochrome Oxidase in Neuronal Metabolism and Alzheimer's Disease. Plenum Press, New York, pp. 1-53.
54. Zhang, C. & Wong-Riley, M. (1999) Expression and regulation of NMDA receptor subunit R1 and neuronal nitric oxide synthase in cortical neuronal cultures: correlation with cytochrome oxidase. J. Neurocytol., 28, 525-539.
55. Zhang, C. & Wong-Riley, M.T. (2000) Depolarizing stimulation upregulates GA-binding protein in neurons: a transcription factor involved in the bigenomic expression of cytochrome oxidase subunits. Eur. J. Neurosci., 12, 1013-1023.