Neuron-specific specificity protein 4 bigenomically regulates the transcription of all mitochondria- and nucleus-encoded cytochrome c oxidase subunit genes in neurons

Journal of Neurochemistry

Volumn 127, Issue 4, 2013, Pages 496-508

  Johar, Kaid ^a   Priya, Anusha ^a   Dhar, Shilpa ^a   Liu, Qiuli ^a   Wong Riley, Margaret T T ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

cytochrome c oxidase; depolarization; mitochondria; Sp4; transcription factor; TTX

Indexed keywords

COMPLEMENTARY DNA; CYTOCHROME C OXIDASE; GLUTAMATE RECEPTOR; MITOCHONDRIAL TRANSCRIPTION FACTOR A; MITOCHONDRIAL TRANSCRIPTION FACTOR B; TRANSCRIPTION FACTOR SP4;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LINE; CELL NUCLEUS; CELL SPECIFICITY; CELL STRAIN N2A; CHROMATIN IMMUNOPRECIPITATION; COX GENE; DNA SYNTHESIS; ENZYME SUBUNIT; GENE OVEREXPRESSION; GENE SILENCING; IMMUNOHISTOCHEMISTRY; MITOCHONDRION; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

CYTOCHROME C OXIDASE; DEPOLARIZATION; MITOCHONDRIA; SP4; TRANSCRIPTION FACTOR; TTX;

ANIMALS; CELL LINE, TUMOR; CELL NUCLEUS; CELLS, CULTURED; DNA-BINDING PROTEINS; ELECTRON TRANSPORT COMPLEX IV; FEMALE; GENE KNOCKDOWN TECHNIQUES; GENOME, MITOCHONDRIAL; HIGH MOBILITY GROUP PROTEINS; MALE; MICE; MICE, INBRED C57BL; NEURONS; PROTEIN BINDING; PROTEIN SUBUNITS; SP4 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; VISUAL CORTEX;

MAMMALIA;

EID: 84887119851     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12433     Document Type: Article

References (51)

1. Arnold S., and, Kadenbach B., (1997) Cell respiration is controlled by ATP, an allosteric inhibitor of cytochrome-c oxidase. Eur. J. Biochem. 249, 350-354.
2. Arnold S., Goglia F., and, Kadenbach B., (1998) 3,5-Diiodothyronine binds to subunit Va of cytochrome-c oxidase and abolishes the allosteric inhibition of respiration by ATP. Eur. J. Biochem. 252, 325-330.
3. Bender E., and, Kadenbach B., (2000) The allosteric ATP-inhibition of cytochrome c oxidase is reversible switched on by cAMP-dependent phosphorylation. FEBS Lett. 466, 730-734.
4. Cole E. G., and, Gaston K., (1997) A functional YY1 binding site is necessary and sufficient to activate Surf-1 promoter activity in response to serum growth factors. Nucleic Acids Res. 25, 3705-3711.
5. DeYoe E. A., Trusk T. C., and, Wong-Riley M. T. T., (1995) Activity correlates of cytochrome oxidase-defined compartments in granular and supragranular layers of primary visual cortex of the macaque monkey. Vis. Neurosci. 12, 629-639.
6. Dhar S. S., and, Wong-Riley M. T. T., (2009) Coupling of energy metabolism and synaptic transmission at the transcriptional level: Role of nuclear respiratory factor 1 in regulating both cytochrome c oxidase and NMDA glutamate receptor subunit genes. J. Neurosci. 29, 483-492.
7. Dhar S. S., and, Wong-Riley M. T. T., (2011) The kinesin superfamily protein KIF17 is regulated by the same transcription factor (NRF-1) as its cargo NR2B in neurons. Biochim. Biophys. Acta 1813, 403-411.
8. Dhar S. S., Ongwijitwat S., and, Wong-Riley M. T. T., (2008) Nuclear respiratory factor 1 regulates all ten nuclear-encoded subunits of cytochrome c oxidase in neurons. J. Biol. Chem. 283, 3120-3129.
9. Dhar S. S., Ongwijitwat S., and, Wong-Riley M. T. T., (2009) Chromosoms conformation capture of all 13 genomic loci in the transcriptional regulation of the multi-subunit bigenomic cytochrome c oxidase in neurons. J. Biol. Chem. 284, 18644-18650.
10. Dhar S. S., Johar K., and, Wong-Riley M. T., (2013) Bigenomic transcriptional regulation of all thirteen cytochrome c oxidase subunit genes by specificity protein 1. Open Biol. 3, 120176.
11. - stoichiometry of cytochrome c oxidase from bovine heart by intramitochondrial ATP/ADP ratios. FEBS Lett. 382, 121-124.
12. 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.
13. Göllner H., Bouwman P., Mangold M., et al,. (2001) Complex phenotype of mice homozygous for a null mutation in the Sp4 transcription factor gene. Genes Cells 6, 689-697.
14. Grossman L. I., and, Lomax M. I., (1997) Nuclear genes for cytochrome c oxidase. Biochim. Biophys. Acta 1352, 174-192.
15. Hevner R. F., and, Wong-Riley M. T. T., (1989) Brain cytochrome oxidase: purification, antibody production and immunohistochemical/histochemical correlations in the CNS. J. Neurosci. 9, 3884-3898.
16. 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.
17. Hüttermann M., Kadenbach B., and, Grossman L. I., (2001) Mammalian subunit IV isoforms of cytochrome c oxidase. Gene 267, 111-1213.
18. Hüttermann M., Schmidt T. R., and, Grossman L. I., (2003) A third isoform of cytochrome c oxidase subunit VIII is present in mammals. Gene 312, 95-102.
19. +-ATPase by nuclear respiratory factor 1. Implication in the tight coupling of neuronal activity, energy generation, and energy consumption. J. Biol. Chem. 287, 40381-40390.
20. 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 electrophoretic procedure. Anal. Biochem. 129, 517-521.
21. Kadenbach B., Stroh A., Becker A., Eckerskorn C., and, Lottspeich F., (1990) Tissue- and species-specific expression of cytochrome c oxidase isozymes in vertebrates. Biochim. Biophys. Acta 1015, 368-372.
22. Kadenbach B., Hüttemann M., Arnold S., Lee I., and, Bender E., (2000) Mitochondrial energy metabolism is regulated via nuclear-coded subunits of cytochrome c oxidase. Free Radic. Biol. Med. 29, 211-221.
23. Li L., and, Davie J. R., (2010) The role of Sp1 and Sp3 in normal and cancer cell biology. Ann. Anat. 192, 275-283.
24. Liang H. L., and, Wong-Riley M. T. T., (2006) Activity-dependent regulation of nuclear respiratory factor-1, nuclear respiratory factor-2 and peroxisome proliferator-activated receptor gamma coactivator-1 in neurons. NeuroReport 17, 401-405.
25. 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. Neuroscience 140, 177-190.
26. Liang H. L., Dhar S. S., and, Wong-Riley M. T. T., (2010) p38 mitogen-activated protein kinase and calcium channels mediate signaling in depolarization-induced activation of peroxisome proliferator-activated receptor gamma coactivator-1alpha in neurons. J. Neurosci. Res. 88, 640-649.
27. Livak K. J., and, Schmittgen T. D., (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408.
28. Mao X., Moerman-Herzog A. M., Wang W., and, Barger S. W., (2006) Differential transcriptional control of the superoxide dismutase-2 kappa B element in neurons and astrocytes. J. Biol. Chem. 281, 35863-35872.
29. Mao X., Yang S. H., Simpkins J. W., and, Barger S. W., (2007) Glutamate receptor activation evokes calpain-mediated degradation of Sp3 and Sp4, the prominent Sp-family transcription factors in neurons. J. Neurochem. 100, 1300-1314.
30. Mao X., Moerman-Herzog A. M., Chen Y., and, Barger S. W., (2009) Unique aspects of transcriptional regulation in neurons-nuances in NFkappaB and Sp1-related factors. J. Neuroinflammation 6, 16.
31. Marin M., Karis A., Visser P., Grosveld F., and, Philipsen S., (1997) Transcription factor Sp1 is essential for early embryonic development but dispensable for cell growth and differentiation. Cell 89, 619-628.
32. Napiwotzki J., Shinzawa-Itoh K., Yoshikawa S., and, Kadenbach B., (1997) ATP and ADP bind to cytochrome c oxidase and regulate its activity. Biol. Chem. 378, 1013-1021.
33. 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.
34. 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.
35. 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.
36. Priya A., Johar K., and, Wong-Riley M. T. T., (2013a) Nuclear respiratory factor 2 regulates the expression of the same NMDA receptor subunit genes as NRF-1: both factors act by a concurrent and parallel mechanism to couple energy metabolism and synaptic transmission. Biochim. Biophys. Acta 1833, 48-58.
37. Priya A., Johar K., and, Wong-Riley M. T. T., (2013b) Specificity protein 4 functionally regulates the transcription of NMDA receptor subunits GluN1, GluN2A, and GluN2B. Biochim. Biophys. Acta 1833, 2745-2756.
38. Ramos B., Valin A., Sun X., and, Gill G., (2009) Sp4-dependent repression of neurotrophin-3 limits dendritic branching. Mol. Cell. Neurosci. 42, 152-159.
39. Safe S., and, Abdelrahim M., (2005) Sp transcription factor family and its role in cancer. Eur. J. Cancer 41, 2438-2448.
40. Scarpulla R. C., (2008) Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1-related coactivator. Ann. N. Y. Acad. Sci. 1147, 321-334.
41. Suske G., (1999) The Sp-family of transcription factors. Gene 238, 291-300.
42. Tsukihara T., Aoyama H., Yamashita E., Tomizaki T., Yamaguchi H., Shinzawa-Itoh K., Nakashima R., Yaono R., and, Yoshikawa S., (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science 272, 1136-1144.
43. 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.
44. Wierstra I., (2008) Sp1: emerging roles-beyond constitutive activation of TATA-less housekeeping genes. Biochem. Biophys. Res. Commun. 372, 1-13.
45. Wikström M., Krab K., and, Saraste M., (1981) Cytochrome Oxidase. A Synthesis. Academic Press, New York.
46. Wong-Riley M., (1979) Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res. 171, 11-28.
47. Wong-Riley M. T. T., (1989) Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci. 12, 94-101.
48. Wong-Riley M. T. T., (2012) Bigenomic regulation of cytochrome c oxidase in neurons and the tight coupling between neuronal activity and energy metabolism. Adv. Exp. Med. Biol. 748, 283-304.
49. Wong-Riley M., Anderson B., Liebl W., and, Huang Z., (1998) Neurochemical organization of the macaque striate cortex: correlation of cytochrome oxidase with Na+K+ATPase, NADPH-diaphorase, nitric oxide synthase, and NMDA receptor subunit 1. Neuroscience 83, 1025-1045.
50. Wu Z., Puigserver P., Andersson U., et al,. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115-124.
51. 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. Neuroscience 141, 1181-1192.