Specificity protein 4 functionally regulates the transcription of NMDA receptor subunits GluN1, GluN2A, and GluN2B

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 12, 2013, Pages 2745-2756

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

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Gene regulation; GluN1; GluN2A; GluN2B; NMDA; Sp4

Indexed keywords

IONOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR GLUN1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR GLUN2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR GLUN2B; NUCLEAR RESPIRATORY FACTOR 1; TRANSCRIPTION FACTOR SP4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; COMPUTER MODEL; ENERGY METABOLISM; GENE CONTROL; MOUSE; MUTAGENESIS; NEUROBLASTOMA CELL; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; SYNAPTIC TRANSMISSION; TRANSCRIPTION REGULATION;

EID: 84882799217     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.07.002     Document Type: Article

References (45)

1. McBain C.J., Mayer M.L. N-Methyl-d-aspartic acid receptor structure and function. Physiol. Rev. 1994, 74:723-760.
2. Hollmann M., Heinemann S. Cloned glutamate receptors. Annu. Rev. Neurosci. 1994, 17:31-108.
3. Behe P., Stern P., Wyllie D.J., Nassar M., Schoepfer R., Colquhoun D. Determination of NMDA NR1 subunit copy number in recombinant NMDA receptors. Proc. Biol. Sci. 1995, 262:205-213.
4. Nakanishi S. Molecular diversity of glutamate receptors and implications for brain function. Science 1992, 258:597-603.
5. Cull-Candy S., Brickley S., Farrant M. NMDA receptor subunits: diversity, development and disease. Curr. Opin. Neurobiol. 2001, 11:327-335.
6. 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.
7. 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.
8. 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.
9. 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.
10. 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.
11. Suske G. The Sp-family of transcription factors. Gene 1999, 238:291-300.
12. Letovsky J., Dynan W.S. Measurement of the binding of transcription factor Sp1 to a single GC box recognition sequence. Nucleic Acids Res. 1989, 17:2639-2653.
13. 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.
14. 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.
15. Dhar S.S., Johar K., Wong-Riley M.T. Bigenomic transcriptional regulation of all thirteen cytochrome c oxidase subunit genes by specificity protein 1. Open Biol. 2013, 3:120176.
16. Ongwijitwat S., Wong-Riley M.T. Functional analysis of the rat cytochrome c oxidase subunit 6A1 promoter in primary neurons. Gene 2004, 337:163-171.
17. Abmayr S.M., Yao T., Parmely T., Workman J.L. Preparation of nuclear and cytoplasmic extracts from mammalian cells. Curr. Protoc. Mol. Biol. 2006, 2. (Chapter 12, Unit 12.1.1).
18. Xia T., Zeng G., Gao L., Yu R.K. Sp1 and AP2 enhance promoter activity of the mouse GM3-synthase gene. Gene 2005, 351:109-118.
19. Ishimaru N., Tabuchi A., Hara D., Hayashi H., Sugimoto T., Yasuhara M., Shiota J., Tsuda M. Regulation of neurotrophin-3 gene transcription by Sp3 and Sp4 in neurons. J. Neurochem. 2007, 100:520-531.
20. 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.
21. Infantino V., Convertini P., Iacobazzi F., Pisano I., Scarcia P., Iacobazzi V. Identification of a novel Sp1 splice variant as a strong transcriptional activator. Biochem. Biophys. Res. Commun. 2011, 412:86-91.
22. Kennett S.B., Udvadia A.J., Horowitz J.M. Sp3 encodes multiple proteins that differ in their capacity to stimulate or repress transcription. Nucleic Acids Res. 1997, 25:3110-3117.
23. Tan N.Y., Khachigian L.M. Sp1 phosphorylation and its regulation of gene transcription. Mol. Cell. Biol. 2009, 29:2483-2488.
24. Sprengel R., Suchanek B., Amico C., Brusa R., Burnashev N., Rozov A., Hvalby O., Jensen V., Paulsen O., Andersen P., Kim J.J., Thompson R.F., Sun W., Webster L.C., Grant S.G., Eilers J., Konnerth A., Li J., McNamara J.O., Seeburg P.H. Importance of the intracellular domain of NR2 subunits for NMDA receptor function in vivo. Cell 1998, 92:279-289.
25. Tang Y.P., Shimizu E., Dube G.R., Rampon C., Kerchner G.A., Zhuo M., Liu G., Tsien J.Z. Genetic enhancement of learning and memory in mice. Nature 1999, 401:63-69.
26. Wang C.C., Held R.G., Chang S.C., Yang L., Delpire E., Ghosh A., Hall B.J. A critical role for GluN2B-containing NMDA receptors in cortical development and function. Neuron 2011, 72:789-805.
27. El Gaamouch F., Buisson A., Moustie O., Lemieux M., Labrecque S., Bontempi B., De Koninck P., Nicole O. Interaction between alphaCaMKII and GluN2B controls ERK-dependent plasticity. J. Neurosci. 2012, 32:10767-10779.
28. Pina-Crespo J.C., Talantova M., Micu I., States B., Chen H.S., Tu S., Nakanishi N., Tong G., Zhang D., Heinemann S.F., Zamponi G.W., Stys P.K., Lipton S.A. Excitatory glycine responses of CNS myelin mediated by NR1/NR3 "NMDA" receptor subunits. J. Neurosci. 2010, 30:11501-11505.
29. Zhou X., Long J.M., Geyer M.A., Masliah E., Kelsoe J.R., Wynshaw-Boris A., Chien K.R. Reduced expression of the Sp4 gene in mice causes deficits in sensorimotor gating and memory associated with hippocampal vacuolization. Mol. Psychiatry 2005, 10:393-406.
30. Mao X., Yang S.H., Simpkins J.W., Barger S.W. Glutamate receptor activation evokes calpain-mediated degradation of Sp3 and Sp4, the prominent Sp-family transcription factors in neurons. J. Neurochem. 2007, 100:1300-1314.
31. Okamoto S., Sherman K., Bai G., Lipton S.A. Effect of the ubiquitous transcription factors, SP1 and MAZ, on NMDA receptor subunit type 1 (NR1) expression during neuronal differentiation. Brain Res. Mol. Brain Res. 2002, 107:89-96.
32. Sowa Y., Shiio Y., Fujita T., Matsumoto T., Okuyama Y., Kato D., Inoue J., Sawada J., Goto M., Watanabe H., Handa H., Sakai T. Retinoblastoma binding factor 1 site in the core promoter region of the human RB gene is activated by hGABP/E4TF1. Cancer Res. 1997, 57:3145-3148.
33. Tovar K.R., Westbrook G.L. The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J. Neurosci. 1999, 19:4180-4188.
34. Choo A.M., Geddes-Klein D.M., Hockenberry A., Scarsella D., Mesfin M.N., Singh P., Patel T.P., Meaney D.F. NR2A and NR2B subunits differentially mediate MAP kinase signaling and mitochondrial morphology following excitotoxic insult. Neurochem. Int. 2012, 60:506-516.
35. Massey P.V., Johnson B.E., Moult P.R., Auberson Y.P., Brown M.W., Molnar E., Collingridge G.L., Bashir Z.I. Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J. Neurosci. 2004, 24:7821-7828.
36. Bartlett T.E., Bannister N.J., Collett V.J., Dargan S.L., Massey P.V., Bortolotto Z.A., Fitzjohn S.M., Bashir Z.I., Collingridge G.L., Lodge D. Differential roles of NR2A and NR2B-containing NMDA receptors in LTP and LTD in the CA1 region of two-week old rat hippocampus. Neuropharmacology 2007, 52:60-70.
37. Foster K.A., McLaughlin N., Edbauer D., Phillips M., Bolton A., Constantine-Paton M., Sheng M. Distinct roles of NR2A and NR2B cytoplasmic tails in long-term potentiation. J. Neurosci. 2010, 30:2676-2685.
38. Cui Z., Feng R., Jacobs S., Duan Y., Wang H., Cao X., Tsien J.Z. Increased NR2A:NR2B ratio compresses long-term depression range and constrains long-term memory. Sci. Rep. 2013, 3:1036.
39. Zhou Y., Takahashi E., Li W., Halt A., Wiltgen B., Ehninger D., Li G.D., Hell J.W., Kennedy M.B., Silva A.J. Interactions between the NR2B receptor and CaMKII modulate synaptic plasticity and spatial learning. J. Neurosci. 2007, 27:13843-13853.
40. Liu Y., Wong T.P., Aarts M., Rooyakkers A., Liu L., Lai T.W., Wu D.C., Lu J., Tymianski M., Craig A.M., Wang Y.T. NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo. J. Neurosci. 2007, 27:2846-2857.
41. Liu A., Zhuang Z., Hoffman P.W., Bai G. Functional analysis of the rat N-methyl-d-aspartate receptor 2A promoter: multiple transcription starts points, positive regulation by Sp factors, and translational regulation. J. Biol. Chem. 2003, 278:26423-26434.
42. Klein M., Pieri I., Uhlmann F., Pfizenmaier K., Eisel U. Cloning and characterization of promoter and 5'-UTR of the NMDA receptor subunit epsilon 2: evidence for alternative splicing of 5'-non-coding exon. Gene 1998, 208:259-269.
43. Hardingham G.E., Bading H. Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat. Rev. Neurosci. 2010, 11:682-696.
44. 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.
45. Wong-Riley M.T. Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci. 1989, 12:94-101.