Nuclear respiratory factor 2 regulates the transcription of AMPA receptor subunit GluA2 (Gria2)

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 12, 2014, Pages 3018-3028

  Priya, Anusha ^a   Johar, Kaid ^a   Nair, Bindu ^a   Wong Riley, Margaret T T ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

AMPA receptor; GABP; Gene regulation; GluA2; Nuclear respiratory factor 2; Transcription factor

Indexed keywords

AMPA RECEPTOR; GA BINDING PROTEIN; GRIA2 PROTEIN; NUCLEAR RESPIRATORY FACTOR 1; RNA; TRANSCRIPTION FACTOR SP4; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ELECTROPHORETIC MOBILITY; ENERGY METABOLISM; GENE MUTATION; HUMAN; MOUSE; NERVE CELL; NEUROBLASTOMA CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; RAT; REAL TIME POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

EID: 84907864669     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.09.006     Document Type: Article

References (61)

1. Isaac J.T., Ashby M.C., McBain C.J. The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 2007, 54:859-871.
2. Malinow R., Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 2002, 25:103-126.
3. Turrigiano G.G. The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 2008, 135:422-435.
4. Shepherd J.D., Huganir R.L. The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu. Rev. Cell Dev. Biol. 2007, 23:613-643.
5. Borges K., Dingledine R. AMPA receptors: molecular and functional diversity. Prog. Brain Res. 1998, 116:153-170.
6. Wenthold R.J., Petralia R.S., Blahos J., Niedzielski A.S. Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J. Neurosci. 1996, 16:1982-1989.
7. Craig A.M., Blackstone C.D., Huganir R.L., Banker G. The distribution of glutamate receptors in cultured rat hippocampal neurons: postsynaptic clustering of AMPA-selective subunits. Neuron 1993, 10:1055-1068.
8. Petralia R.S., Wenthold R.J. Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J. Comp. Neurol. 1992, 318:329-354.
9. Zhu J.J., Esteban J.A., Hayashi Y., Malinow R. Postnatal synaptic potentiation: delivery of GluR4-containing AMPA receptors by spontaneous activity. Nat. Neurosci. 2000, 3:1098-1106.
10. Wong-Riley M.T. Bigenomic regulation of cytochrome C oxidase in neurons and the tight coupling between neuronal activity and energy metabolism. Adv. Exp. Med. Biol. 2012, 748:283-304.
11. Wong-Riley M.T. Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci. 1989, 12:94-101.
12. Priya A., Johar K., Nair B., Wong-Riley M.T. Specificity protein 4 (Sp4) regulates the transcription of AMPA receptor subunit GluA2 (Gria2). Biochim. Biophys. Acta 2014, 1843:1196-1206.
13. Dhar S.S., Liang H.L., Wong-Riley M.T. Nuclear respiratory factor 1 co-regulates AMPA glutamate receptor subunit 2 and cytochrome c oxidase: tight coupling of glutamatergic transmission and energy metabolism in neurons. J. Neurochem. 2009, 108:1595-1606.
14. Dhar S.S., Ongwijitwat S., Wong-Riley M.T. Nuclear respiratory factor 1 regulates all ten nuclear-encoded subunits of cytochrome c oxidase in neurons. J. Biol. Chem. 2008, 283:3120-3129.
15. Dhar S.S., Wong-Riley M.T. 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. 2009, 29:483-492.
16. Johar K., Priya A., Dhar S., Liu Q., Wong-Riley M.T. Neuron-specific specificity protein 4 bigenomically regulates the transcription of all mitochondria- and nucleus-encoded cytochrome c oxidase subunit genes in neurons. J. Neurochem. 2013, 127:496-508.
17. Priya A., Johar K., Wong-Riley M.T. Specificity protein 4 functionally regulates the transcription of NMDA receptor subunits GluN1, GluN2A, and GluN2B. Biochim. Biophys. Acta 2013, 1833:2745-2756.
18. Ongwijitwat S., Liang H.L., Graboyes E.M., Wong-Riley M.T. Nuclear respiratory factor 2 senses changing cellular energy demands and its silencing down-regulates cytochrome oxidase and other target gene mRNAs. Gene 2006, 374:39-49.
19. Ongwijitwat S., Wong-Riley M.T. Is nuclear respiratory factor 2 a master transcriptional coordinator for all ten nuclear-encoded cytochrome c oxidase subunits in neurons?. Gene 2005, 360:65-77.
20. Priya A., Johar K., Wong-Riley M.T. 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 2013, 1833:48-58.
21. Abmayr S.M., Yao T., Parmely T., Workman J.L. Preparation of nuclear and cytoplasmic extracts from mammalian cells. Curr. Protoc. Mol. Biol. 2006, (Chapter 12 (2006) Unit 12.1).
22. Dhar S.S., Liang H.L., Wong-Riley M.T. Transcriptional coupling of synaptic transmission and energy metabolism: role of nuclear respiratory factor 1 in co-regulating neuronal nitric oxide synthase and cytochrome c oxidase genes in neurons. Biochim. Biophys. Acta 2009, 1793:1604-1613.
23. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
24. 2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 1995, 15:193-204.
25. Sans N., Vissel B., Petralia R.S., Wang Y.X., Chang K., Royle G.A., Wang C.Y., O'Gorman S., Heinemann S.F., Wenthold R.J. Aberrant formation of glutamate receptor complexes in hippocampal neurons of mice lacking the GluR2 AMPA receptor subunit. J. Neurosci. 2003, 23:9367-9373.
26. Sommer B., Kohler M., Sprengel R., Seeburg P.H. RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 1991, 67:11-19.
27. Higuchi M., Single F.N., Kohler M., Sommer B., Sprengel R., Seeburg P.H. RNA editing of AMPA receptor subunit GluR-B: a base-paired intron-exon structure determines position and efficiency. Cell 1993, 75:1361-1370.
28. Dingledine R., Borges K., Bowie D., Traynelis S.F. The glutamate receptor ion channels. Pharmacol. Rev. 1999, 51:7-61.
29. Laezza F., Dingledine R. Voltage-controlled plasticity at GluR2-deficient synapses onto hippocampal interneurons. J. Neurophysiol. 2004, 92:3575-3581.
30. Hestrin S. Different glutamate receptor channels mediate fast excitatory synaptic currents in inhibitory and excitatory cortical neurons. Neuron 1993, 11:1083-1091.
31. Kamboj S.K., Swanson G.T., Cull-Candy S.G. Intracellular spermine confers rectification on rat calcium-permeable AMPA and kainate receptors. J. Physiol. 1995, 486(Pt 2):297-303.
32. Gerlai R., Henderson J.T., Roder J.C., Jia Z. Multiple behavioral anomalies in GluR2 mutant mice exhibiting enhanced LTP. Behav. Brain Res. 1998, 95:37-45.
33. Liu S.Q., Cull-Candy S.G. Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature 2000, 405:454-458.
34. Liu S.J., Cull-Candy S.G. Activity-dependent change in AMPA receptor properties in cerebellar stellate cells. J. Neurosci. 2002, 22:3881-3889.
35. Plant K., Pelkey K.A., Bortolotto Z.A., Morita D., Terashima A., McBain C.J., Collingridge G.L., Isaac J.T. Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat. Neurosci. 2006, 9:602-604.
36. Chung H.J., Steinberg J.P., Huganir R.L., Linden D.J. Requirement of AMPA receptor GluR2 phosphorylation for cerebellar long-term depression. Science 2003, 300:1751-1755.
37. Toyoda H., Wu L.J., Zhao M.G., Xu H., Jia Z., Zhuo M. Long-term depression requires postsynaptic AMPA GluR2 receptor in adult mouse cingulate cortex. J. Cell. Physiol. 2007, 211:336-343.
38. Bai X., Wong-Riley M.T. Neuronal activity regulates protein and gene expressions of GluR2 in postnatal rat visual cortical neurons in culture. J. Neurocytol. 2003, 32:71-78.
39. Wong-Riley M.T., Jacobs P. AMPA glutamate receptor subunit 2 in normal and visually deprived macaque visual cortex. Vis. Neurosci. 2002, 19:563-573.
40. Rosmarin A.G., Resendes K.K., Yang Z., McMillan J.N., Fleming S.L. GA-binding protein transcription factor: a review of GABP as an integrator of intracellular signaling and protein-protein interactions. Blood Cells Mol. Dis. 2004, 32:143-154.
41. Batchelor A.H., Piper D.E., de la Brousse F.C., McKnight S.L., Wolberger C. The structure of GABPalpha/beta: an ETS domain-ankyrin repeat heterodimer bound to DNA. Science 1998, 279:1037-1041.
42. LaMarco K., Thompson C.C., Byers B.P., Walton E.M., McKnight S.L. Identification of Ets- and notch-related subunits in GA binding protein. Science 1991, 253:789-792.
43. de la Brousse F.C., Birkenmeier E.H., King D.S., Rowe L.B., McKnight S.L. Molecular and genetic characterization of GABP beta. Genes Dev. 1994, 8:1853-1865.
44. Yang S.J., Liang H.L., Ning G., Wong-Riley M.T. Ultrastructural study of depolarization-induced translocation of NRF-2 transcription factor in cultured rat visual cortical neurons. Eur. J. Neurosci. 2004, 19:1153-1162.
45. Wong-Riley M.T., Yang S.J., Liang H.L., Ning G., Jacobs P. Quantitative immuno-electron microscopic analysis of nuclear respiratory factor 2 alpha and beta subunits: normal distribution and activity-dependent regulation in mammalian visual cortex. Vis. Neurosci. 2005, 22:1-18.
46. Zhang C., Wong-Riley M.T. Depolarizing stimulation upregulates GA-binding protein in neurons: a transcription factor involved in the bigenomic expression of cytochrome oxidase subunits. Eur. J. Neurosci. 2000, 12:1013-1023.
47. 2+ influx in hippocampal CA1 neurons of gerbil. J. Neurosci. 1997, 17:6179-6188.
48. 2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci. 2007, 30:126-134.
49. Buckingham S.D., Kwak S., Jones A.K., Blackshaw S.E., Sattelle D.B. Edited GluR2, a gatekeeper for motor neurone survival?. Bioessays 2008, 30:1185-1192.
50. Kwak S., Weiss J.H. Calcium-permeable AMPA channels in neurodegenerative disease and ischemia. Curr. Opin. Neurobiol. 2006, 16:281-287.
51. Gollner H., Bouwman P., Mangold M., Karis A., Braun H., Rohner I., Del Rey A., Besedovsky H.O., Meinhardt A., van den Broek M., Cutforth T., Grosveld F., Philipsen S., Suske G. Complex phenotype of mice homozygous for a null mutation in the Sp4 transcription factor gene. Genes Cells 2001, 6:689-697.
52. Supp D.M., Witte D.P., Branford W.W., Smith E.P., Potter S.S. Sp4, a member of the Sp1-family of zinc finger transcription factors, is required for normal murine growth, viability, and male fertility. Dev. Biol. 1996, 176:284-299.
53. Nie F., Wong-Riley M. Nuclear respiratory factor-2 subunit protein: correlation with cytochrome oxydase and regulation by functional activity in the monkey primary visual cortex. J. Comp. Neurol. 1999, 404:310-320.
54. Guo A., Nie F., Wong-Riley M. 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. 2000, 417:221-232.
55. Wu Z., Puigserver P., Andersson U., Zhang C., Adelmant G., Mootha V., Troy A., Cinti S., Lowell B., Scarpulla R.C., Spiegelman B.M. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 1999, 98:115-124.
56. Meng H., Liang H.L., Wong-Riley M. Quantitative immuno-electron microscopic analysis of depolarization-induced expression of PGC-1alpha in cultured rat visual cortical neurons. Brain Res. 2007, 1175:10-16.
57. Liang H.L., Dhar S.S., Wong-Riley M.T. 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. 2010, 88:640-649.
58. Vercauteren K., Gleyzer N., Scarpulla R.C. PGC-1-related coactivator complexes with HCF-1 and NRF-2beta in mediating NRF-2(GABP)-dependent respiratory gene expression. J. Biol. Chem. 2008, 283:12102-12111.
59. Gunther M., Laithier M., Brison O. A set of proteins interacting with transcription factor Sp1 identified in a two-hybrid screening. Mol. Cell. Biochem. 2000, 210:131-142.
60. Dhar S.S., Wong-Riley M.T. Chromosome conformation capture of transcriptional interactions between cytochrome c oxidase genes and genes of glutamatergic synaptic transmission in neurons. J. Neurochem. 2010, 115:676-683.
61. Johar K., Priya A., Wong-Riley M.T. Regulation of Na(+)/K(+)-ATPase by neuron-specific transcription factor Sp4: implication in the tight coupling of energy production, neuronal activity and energy consumption in neurons. Eur. J. Neurosci. 2013, 39:566-578.