Activity-dependent bigenomic transcriptional regulation of cytochrome c oxidase in neurons

Transcriptional Regulation by Neuronal Activity: To the Nucleus and Back

Volumn , Issue , 2008, Pages 209-228

  Wong Riley, Margaret T T ^a   Liang, Huan Ling ^a   Ongwijitwat, Sakkapol ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77953807154     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-0-387-73609-9_11     Document Type: Chapter

References (87)

1. Anderson, S., Bankier, A.T., Barrell, B.G., de Bruijn, M.H., Coulson, A.R., Drouin, J., Eperon, I.C., Nierlich, D.P., Roe, B.A., Sanger, F., Schreier, P.H., Smith, A.J., Staden, R. and Young, I.G. (1981) Sequence and organization of the human mitochondrial genome. Nature 290, 457-465.
2. Andersson, U. and Scarpulla, R.C. (2001) PGC-1-related coactivator, a novel, serum-inducible coactivator of nuclear respiratory factor 1-dependent transcription in mammalian cells. Mol. Cell Biol. 21, 3738-3749.
3. Arany, Z., Novikov, M., Chin, S., Ma, Y., Rosenzweig, A. and Speigelman, B.M. (2006) Transverse aortic constriction leads to accelerated heart failure in mice lacking PPAR-γ coactivator 1α. Proc. Natl. Acad. Sci. 103, 10086-10091.
4. Baar, K., Wende, A.R., Jones, T.E., Marison, M., Nolte, L.A., Chen, M., Kelly, D.P. and Holloszy, J.O. (2002) Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. Faseb. J. 16, 1879-1886.
5. Bachman, N.J., Yang, T.L., Dasen, J.S., Ernst, R.E. and Lomax, M.I. (1996) Phylogenetic footprinting of the human cytochrome c oxidase subunit VB promoter. Arch. Biochem. Biophys. 333, 152-162.
6. Basu, A., Park, K., Atchison, M.L., Carter, R.S. and 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 Sp1. J. Biol. Chem. 268, 4188-4196.
7. Bengtsson, J., Gustafsson, T., Widegren, U., Jansson, E. and Sundberg, C. (2001) Mitochondrial transcription factor A and respiratory complex IV increase in response to exercise training in humans. Pflugers Arch. 443, 61-66.
8. Carter, R.S. and 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.. and 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. Chantrel-Groussard, K., Deply, L., Ratinaud, M.H. and Cogne, M. (2001) Characterization of the murine gene for subunit VIIaL of cytochrome c oxidase. C.R. Adem. Sci. III 324, 1117-1123.
11. Chaudhuri, A., Matsubara, J.A. and Cynader, M.S. (1995) Neuronal activity in primate visual cortex assessed by immunostaining for the transcription factor Zif268. Vis. Neurosci. 12, 35-50.
12. Clayton, D.A. (1991) Replication and transcription of vertebrate mitochondrial DNA. Annu. Rev. Cell Biol. 7, 409-435.
13. Clayton, D.A. (2000) Transcription and replication of mitochondrial DNA. Hum. Reprod. 15 Suppl. 2 11-17.
14. Dairaghi, D.J., Shadel, G.S. and Clayton, D.A. (1995) Addition of a 29 residue carboxyl-terminal tail converts a simple HMG box-containing protein into a transcriptional activator. J. Mol. Biol. 249, 11-28.
15. Ekstrand, M.I., Falkenberg, M., Rantanen, A., Park, C.B., Gaspari, M., Hultenby, K., Rustin, P., Gustafsson, C.M. and Larsson, N.G. (2004) Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Human Mol. Genetics 13, 935-944.
16. Evans, M.J. and Scarpulla, R.C. (1989) Interaction of nuclear factors with multiple sites in the somatic cytochrome c promoter. Characterization of upstream NRF-1, ATF, and intron Sp1 recognition sequences. J. Biol. Chem. 264, 14361-14368.
17. Evans, M.J. and Scarpulla, R.C. (1990) NRF-1: A trans-activator of nuclear-encoded respiratory genes in animal cells. Genes Dev. 4, 1023-1034.
18. Falkenberg, M., Gaspari, M., Rantanen, A., Trifunovic, A., Larsson, N.G. and Gustafsson, C.M. (2002) Mitochondrial transcription factors B1 and B2 activate transcription of human mtDNA. Nat. Genet. 31, 289-294.
19. Fisher, R.P. and Clayton, D.A. (1988) Purification and characterization of human mitochondrial transcription factor 1. Mol. Cell Biol. 8, 3496-3509.
20. Gleyzer, N., Vercauteren, K. and Scarpulla, R.C. (2005) Control of mitochondrial transcription specificity factors (TFB1M and TFB2M) by nuclear respiratory factors (NRF-1 and NRF-2) and PGC-1 family coactivators. Mol. Cell Biol. 25, 1354-1366.
21. Gopalakrishnan, L. and Scarpulla, R.C. (1995) Structure, expression, and chromosomal assignment of the human gene encoding nuclear respiratory factor 1. J. Biol. Chem. 270, 18019-18025.
22. Goto, M., Terada, S., Kato, M., Katoh, M., Yokozeki, T., Tabata, I. and Shimokawa, T. (2000) cDNA Cloning and mRNA analysis of PGC-1 in epitrochlearis muscle in swimming-exercised rats. Biochem. Biophys. Res. Commun. 274, 350-354.
23. Gordon, J.W., Rungi, A.A., Inagaki, H. and Hood, D.A. (2001) Effects of contractile activity on mitochondrial transcription factor A expression in skeletal muscle. J. Appl. Physiol. 90, 389-396.
24. Grossman, L.I., Lomax, M.I. (1997) Nuclear genes for cytochrome c oxidase. Biochim. Biophys. Acta 1352, 174-192.
25. Gugneja, S., Virbasius, C.M. and Scarpulla, R.C. (1996) Nuclear respiratory factors 1 and 2 utilize similar glutamine-containing clusters of hydrophobic residues to activate transcription. Mol. Cell Biol. 16, 5708-5716.
26. Guo, A.L., Nie, F. and Wong-Riley, M.T.T. (2000) Human brain nuclear respiratory factor (NRF) 2α cDNA: Isolation, subcloning, sequencing and in situ hybridization of transcripts in normal and visually deprived macaque visual system. J. Comp. Neurol. 417, 221-232.
27. Hevner, R.F. and Wong-Riley, M.T.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.
28. Hevner, R.F. and Wong-Riley, M.T.T. (1993) Mitochondrial and nuclear gene expression for cytochrome oxidase subunits are disproportionately regulated by functional activity in neurons. J. Neurosci. 13, 1805-1819.
29. Herdegen, T., Kovary, K., Buhl, A., Bravo, R., Zimmermann, M. and Gass, P. (1995) Basal expression of the inducible transcription factors c-Jun, Jun B, Jun D, c-Fos, Fos B, and Krox-24 in the adult rat brain. J. Comp. Neurol. 354, 39-56.
30. Hoshinaga, H., Amuro, N., Goto, Y. and Okazaki, T. (1994)Molecular cloning and characterization of the rat cytochrome c oxidase subunit Vb gene. J. Biochem. (Tokyo) 115, 194-201.
31. Huo, L. and Scarpulla, R.C. (1999) Multiple 5'-untranslated exons in the nuclear respiratory factor 1 gene span 47 kb and contribute to transcript heterogeneity and translational efficiency. Gene 233, 213-224.
32. Huo, L., Scarpulla, R.C. (2001) Mitochondrial DNA instability and peri-implantation lethality associated with targeted disruption of nuclear respiratory factor 1 in mice. Mol. Cell Biol. 21, 644-654.
33. Hüttemann, M., Muhlenbein, N., Schmidt, T.R., Grossman, L.I. and Kadenbach, B. (2000) Isolation and sequence of the human cytochrome c oxidase subunit VIIaL gene. Biochim. Biophys. Acta 1492, 252-258.
34. Inagaki, H., Kitano, S., Lin, K.H., Maeda, S. and Saito, T. (1998) Inhibition of mitochondrial gene expression by antisense RNA of mitochondrial transcription factor A (mtTFA). Biochem. Mol. Biol. Int. 45, 567-573.
35. Inagaki, H., Hayashi, T., Matsushima, Y., Lin, K.H., Maeda, S., Ichihara, S., Kitagawa, Y. and Saito, T. (2000) Isolation of rat mitochondrial transcription factor A (r-Tfam) cDNA. DNA Seq. 11, 131-135.
36. Irrcher, I., Adhihetty, P.J., Sheehan, T., Joseph, A.M. and Hood, D.A. (2003) PPARgamma coactivator-1alpha expression during thyroid hormone- And contractile activity-induced mitochondrial adaptations. Am. J. Physiol. Cell Physiol. 284, C1669-C1677.
37. Kadenbach, B., Jarausch, J., Hartmann, R. and Merle, P. (1983) Separation of mammalian cytochrome c oxidase into 13 polypeptides by a sodium dodecyl sulfate-gel eletrophoretic procedure. Analyt. Biochem. 129, 517-521.
38. Kadenbach, B., Hüttemann, M., Arnold, S., Lee, I. and Bender, E. (2000) Mitochondrial energy metabolism is regulated via nuclear-cpded subunits of cytochrome c oxidase. Free Rad. Biol. Med. 29, 211-221.
39. Kelly, D.P. and Scarpulla, R.C. (2004) Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 18, 357-368.
40. Knutti, D. and Kralli, A. (2001) PGC-1, a versatile coactivator. Trends Endocrinol. Metab. 12, 360-365.
41. La Marco, K., Thompson, C.C., Byers, B.P., Walton, E.M. and McKnight, S.L. (1991) Identification of Ets- And Notch-related subunits in GA-binding protein. Science 253, 789-792.
42. Larsson, N.G., Barsh, G.S. and Clayton, D.A. (1997) Structure and chromosomal localization of the mouse mitochondrial transcription factor A gene (Tfam). Mamm. Genome 8, 139-140.
43. Larsson, N.G., Wang, J., Wilhelmsson, H., Oldfors, A., Rustin, P., Lewandoski, M., Barsh, G.S. and Clayton, D.A. (1998) Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat. Genet. 18, 231-236.
44. Liang, H.L. and Wong-Riley, M.T.T. (2006) Activity-dependent regulation of nuclear respiratory factor-1, nuclear respiratory factor-2, and peroxisome proliferators-activated receptor gamma coactivator-1 in neurons. Neuro Report 17, 401-405.
45. Liang, H.L., Ongwijitwat, S. and Wong-Riley, M.T.T. (2006) Bigenomic functional regulation of all 13 cytochrome c oxidase subunit transcripts in rat neurons in vitro and in vivo. Neurosci. 140, 177-190.
46. Lin, J., Wu, H., Tarr, P.T., Zhang, C.Y., Wu, Z., Boss, O., Michael, L.F., Puigserver, P., Isotani, E., Olson, E.N., Lowell, B.B., Bassel-Duby, R. and Spiegelman, B.M. (2002) Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418, 797-801.
47. Lin, J., Wu, P.-H., Tarr, P.T., Lindenberg, K.S., St-Pierre, J., Zhang, C.Y., Mootha, V.K., Jäger, S., Vianna, C.R., Reznick, R.M., Cui, L., Manieri, M., Donovan, M.X., Wu, Z., Cooper, M.P., Fan, M.C., Rohas, L.M., Zavacki, A.M., Cinti, S., Shulman, G.I., Lowell, B.B., Krainc, D. and Spiegelman, B.M. (2004) Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1α null mice. Cell 119, 121-135.
48. Liu, S. and Wong-Riley, M.T.T. (1994) Nuclear-encoded mitochondrial precursor protein: Intramitochondrial delivery to dendrites and axon terminals of neurons and regulation by neuronal activity. J. Neurosci. 14, 5338-5351.
49. Lowry, O.H. (1975) Energy metabolism in brain and its control. In: D.H. Ingvar and N.A. Lassen (Eds.), Brain Work. Alfred Benzon Symposium VIII. Academic Press, New York, pp. 377-388.
50. McCulloch, V. and Shadel, G.S. (2003) Human mitochondrial transcription factor B1 interacts with the C-terminal activation region of h-mtTFA and stimulates transcription independent of its RNA methyltransferase activity. Mol. Cell. Biol. 23, 5816-5824.
51. Mell, O.C., Seibel, P. and Kadenbach, B. (1994) Structural organization of the rat genes encoding liver- And heart-type of cytochrome c oxidase subunit VIa and a pseudogene related to the COXVIa-L cDNA. Gene 140, 179-186.
52. Murakami, T., Shimomura, Y., Yoshimura, A., Sokabe, M. and Fujitsuka, N. (1998) Induction of nuclear respiratory factor-1 expression by an acute bout of exercise in rat muscle. Biochim. Biophys. Acta 1381, 113-122.
53. Nie, F. and Wong-Riley, M. (1999) Nuclear respiratory factor-2 subunit protein: Correlation with cytochrome oxidase and regulation by functional activity in the monkey primary visual cortex. J. Comp. Neurol. 404, 310-320.
54. Nisoli, E., Clementi, E., Paolucci, C., Cozzi, V., Tonello, C., Sciorati, C., Bracale, R., Valerio, A., Francolini, M., Moncada, S. and Carruba, M.O. (2003) Mitochondrial biogenesis in mammals: The role of endogenous nitric oxide. Science 299, 896-899.
55. Okuno, H., Kanou, S., Tokuyama, W., Li, Y.X. and Miyashita, Y. (1997) Layer-specific differential regulation of transcription factors Zif268 and Jun-D in visual cortex V1 and V2 of macaque monkeys. Neurosci. 81, 653-666.
56. Ongwijitwat, S. and Wong-Riley, M.T.T. (2004) Functional analysis of the rat cytochrome c oxidase subunit 6A1 promoter in primary neurons. Gene 337, 163-171.
57. Ongwijitwat, S. and Wong-Riley, M.T.T. (2005) Is nuclear respiratory factor 2 a master transcriptional coordinator for all ten nuclear-encoded cytochrome c oxidase subunits in neurons? Gene 360, 65-77.
58. Ongwijitwat, S., Liang, H.L., Graboyes, E.M. and Wong-Riley, M.T.T. (2006) Nuclear respiratory factor 2 senses changing cellular energy demands and its silencing down-regulates cytochrome oxidase and other target gene mRNAs. Gene 374, 39-49.
59. Parisi, M.A. and Clayton, D.A. (1991) Similarity of human mitochondrial transcription factor 1 to high mobility group proteins. Science 252, 965-969.
60. Puigserver, P., Wu, Z., Park, C.W., Graves, R., Wright, M. and Spiegelman, B.M. (1998) A coldinducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92, 829-839.
61. Puigserver, P., Adelmant, G., Wu, Z., Fan, M., Xu, J., O'Malley, B. and Spiegelman, B.M. (1999) Activation of PPARgamma coactivator-1 through transcription factor docking. Science 286, 1368-1371.
62. Puigserver, P. and Spiegelman, B.M. (2003) Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): Transcriptional coactivator and metabolic regulator. Endocr. Rev. 24, 78-90.
63. Scarpulla, R.C. (1997) Nuclear control of respiratory chain expression in mammalian cells. J. Bioenerg. Biomemb. 29, 109-119.
64. Scarpulla, R.C. (2002) Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochim. Biophys. Acta 1576, 1-14.
65. Scarpulla, R.C. (2006) Nuclear control of respiratory gene expression in mammalian cells. J. Cell Biochem. 97, 673-683.
66. Seelan, R.S. and Grossman, L.I. (1997) Structural organization and promoter analysis of the bovine cytochrome c oxidase subunit VIIc gene. A functional role for YY1. J. Biol. Chem. 272, 19175-10181.
67. Seelan, R.S., Gopalakrishnan, L., Scarpulla, R.C. and Grossman, L.I. (1996) Cytochrome c oxidase subunit VIIa liver isoform. Characterization and identification of promoter elements in the bovine gene. J. Biol. Chem. 271, 2112-2120.
68. Short, K.R., Vittone, J.L., Bigelow, M.L., Proctor, D.N., Rizza, R.A., Coenen-Schimke, J.M. and Nair, K.S. (2003) Impact of aerobic exercise training on age-related changes in insulin sensitivity and muscle oxidative capacity. Diabetes 52, 1888-1896.
69. Smith, E.O. and Lomax, M.I. (1993) Structural organization of the bovine gene for the heart/muscle isoform of cytochrome c oxidase subunit VIa. Biochim. Biophys. Acta 1174, 63-71.
70. Sucharov, C., Basu, A., Carter, R.S. and Avadhani, N.G. (1995) A novel transcriptional initiator activity of the GABP factor binding ets sequence repeat from the murine cytochrome c oxidase Vb gene. Gene Expr. 5, 93-111.
71. Takata, K., Inoue, Y.H., Hirose, F., Murakami, S., Shimanouchi, K., Sakimoto, I. and Sakaguchi, K. (2003) Spatio-temporal expression of Drosophila mitochondrial transcription factor A during development. Cell Biol. Int. 27, 361-374.
72. Thompson, C.C., Brown, T.A. and McKnight, S.L. (1991) Convergence of Ets- And Notch-related structural motifs in a heteromeric DNA binding complex. Science 253, 762-768.
73. Tritos, N.A., Mastaitis, J.W., Kokkotou, E.G., Puigserver, P., Spiegelman, B.M. and Maratos-Flier, E. (2003) Characterization of the peroxisome proliferators activated receptor coactivator 1 alpha (PGC 1α) expression in the murine brain. Brain Res. 961, 255-260.
74. Virbasius, J.V. and 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.
75. Virbasius, J.V. and 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.
76. Virbasius, J.V., Virbasius, C.A. and 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. Gene Dev. 7, 380-392.
77. Virbasius, C.A., Virbasius, J.V. and Scarpulla, R.C. (1993b) NRF-1, an activator involved in nuclear-mitochondrial interaction, utilizes a new DNA-binding domain conserved in a family of developmental regulators. Gene Dev. 7, 2431-2445.
78. Wong-Riley, M.T.T. (1989) Cytochrome oxidase: An endogenous metabolic marker for neuronal activity. Trends Neurosci. 12, 94-101.
79. Wong-Riley, M.T.T., Mullen, M.A., Huang, Z. and Guyer, C. (1997) Brain cytochrome oxidase subunit genes: Isolation, subcloning, sequencing, light and EM in situ hybridization of transcripts, and regulation by neuronal activity. Neurosci. 79, 1035-1055.
80. Wong-Riley, M.T.T., Nie, F., Hevner, R.F. and Liu, S. (1998) Brain cytochrome oxidase: Functional significance and bigenomic regulation in the CNS. In: F. Gonzalez-Lima (Ed.) Cytochrome oxidase in neuronal metabolism and Alzheimer's Disease. Plenum Press, New York, PP 1-53.
81. Wong-Riley, M.T.T., Guo, A., Bachman, N.J. and Lomax, M.I. (2000) Human COX6A1 gene: promoter analysis, cDNA isolation and expression in the monkey brain. Gene 247, 63-75.
82. Wong-Riley, M.T.T., Yang, S.J., Liang, H.L., Ning, G. and Jacobs, P. (2005) Quantitative immunoelectron microscopic analysis of nuclear respiratory factor 2 alpha and beta subunits: Normal distribution and activity-dependent regulation in mammalian visual cortex. Visual Neurosci. 22, 1-18.
83. Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R.C. and Spiegelman, B.M. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115-124.
84. Xia, Y., Buja, L.M., Scarpulla, R.C. and McMillin, J.B. (1997) Electrical stimulation of neonatal cardiomyocytes results in the sequential activation of nuclear genes governing mitochondrial proliferation and differentiation. Proc. Natl. Acad. Sci. USA, 94, 11399-11404.
85. Yang, S.J., Liang, H.L., Ning, G. and Wong-Riley, M.T.T. (2004) Ultrastructural study of depolarization-induced translocation of NRF-2 transcription factor in cultured rat visual cortical neurons. Eur. J. Neurosci. 19, 1153-1162.
86. Yang, S.J., Liang, H.L. and Wong-Riley, M.T.T. (2006) Activity-dependent transcriptional regulation of nuclear respiratory factor-1 in cultured rat visual cortical neurons. Neurosci. 141, 1181-1192.
87. Zhang, C., Wong-Riley, M. (2000) Depolarization 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.