Inositol polyphosphate multikinase is a transcriptional coactivator required for immediate early gene induction

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 40, 2013, Pages 16181-16186

  Xu, Risheng ^a   Paul, Bindu D ^a   Smith, Dani R ^b   Tyagi, Richa ^a   Rao, Feng ^a   Khan, A Basit ^a   Blech, Daniel J ^a   Vandiver, M Scott ^a   Harraz, Maged M ^a   Guha, Prasun ^a   Ahmed, Ishrat ^a   Sen, Nilkantha ^c   Gallagher, Michela ^b   Snyder, Solomon H ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Inositol phosphates; Learning

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; INOSITOL POLYPHOSPHATE; INOSITOL POLYPHOSPHATE MULTIKINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; ELECTROCONVULSIVE THERAPY; ENZYME ACTIVITY; ENZYME MECHANISM; EPIGENETICS; GENE DELETION; GENE INDUCTION; GENETIC TRANSCRIPTION; IMMEDIATE EARLY GENE; MEMORY DISORDER; MOUSE; NERVE CELL CULTURE; NERVE CELL PLASTICITY; NONHUMAN; ONCOGENE C FOS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; SPATIAL MEMORY;

INOSITOL PHOSPHATES; LEARNING;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN; CHROMATIN IMMUNOPRECIPITATION; CREB-BINDING PROTEIN; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; GENES, IMMEDIATE-EARLY; MAZE LEARNING; MICE; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); RECOGNITION (PSYCHOLOGY); TRANSCRIPTIONAL ACTIVATION;

EID: 84885086001     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1315551110     Document Type: Article

References (43)

1. Cole AJ, Saffen DW, Baraban JM, Worley PF (1989) Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340(6233):474-476.
2. Curran T, Morgan JI (1985) Superinduction of c-fos by nerve growth factor in the presence of peripherally active benzodiazepines. Science 229(4719):1265-1268.
3. Cole RL, Konradi C, Douglass J, Hyman SE (1995) Neuronal adaptation to amphetamine and dopamine: Molecular mechanisms of prodynorphin gene regulation in rat striatum. Neuron 14(4):813-823.
4. Hope B, Kosofsky B, Hyman SE, Nestler EJ (1992) Regulation of immediate early gene expression and AP-1 binding in the rat nucleus accumbens by chronic cocaine. Proc Natl Acad Sci USA 89(13):5764-5768.
5. Hunt SP, Pini A, Evan G (1987) Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature 328(6131):632-634.
6. Cole AJ, Abu-Shakra S, Saffen DW, Baraban JM, Worley PF (1990) Rapid rise in transcription factor mRNAs in rat brain after electroshock-induced seizures. J Neurochem 55(6):1920-1927.
7. Bozon B, Davis S, Laroche S (2003) A requirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval. Neuron 40(4):695-701.
8. Jones MW, et al. (2001) A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci 4(3):289-296.
9. Ramamoorthi K, et al. (2011) Npas4 regulates a transcriptional program in CA3 required for contextual memory formation. Science 334(6063):1669-1675.
10. Alberi L, et al. (2011) Activity-induced Notch signaling in neurons requires Arc/Arg3.1 and is essential for synaptic plasticity in hippocampal networks. Neuron 69(3):437-444.
11. Plath N, et al. (2006) Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52(3):437-444.
12. Saiardi A, Erdjument-Bromage H, Snowman AM, Tempst P, Snyder SH (1999) Synthesis of diphosphoinositol pentakisphosphate by a newly identified family of higher inositol polyphosphate kinases. Curr Biol 9(22):1323-1326.
13. Saiardi A, et al. (2001) Mammalian inositol polyphosphate multikinase synthesizes inositol 1,4,5-trisphosphate and an inositol pyrophosphate. Proc Natl Acad Sci USA 98(5):2306-2311.
14. Maag D, et al. (2011) Inositol polyphosphate multikinase is a physiologic PI3-kinase that activates Akt/PKB. Proc Natl Acad Sci USA 108(4):1391-1396.
15. Resnick AC, et al. (2005) Inositol polyphosphate multikinase is a nuclear PI3-kinase with transcriptional regulatory activity. Proc Natl Acad Sci USA 102(36):12783-12788.
16. Kim S, et al. (2011) Amino acid signaling to mTOR mediated by inositol polyphosphate multikinase. Cell Metab 13(2):215-221.
17. Xu R, et al. (2013) Inositol polyphosphate multikinase is a coactivator of p53-mediated transcription and cell death. Sci Signal 6(269):ra22.
18. Xu R, Snyder SH (2013) Gene transcription by p53 requires inositol polyphosphate multikinase as a co-activator. Cell Cycle 12(12):1819-1820.
19. Frederick JP, et al. (2005) An essential role for an inositol polyphosphate multikinase, Ipk2, in mouse embryogenesis and second messenger production. Proc Natl Acad Sci USA 102(24):8454-8459.
20. Tronche F, et al. (1999) Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23(1):99-103.
21. Zhu Y, et al. (2001) Ablation of NF1 function in neurons induces abnormal development of cerebral cortex and reactive gliosis in the brain. Genes Dev 15(7): 859-876.
22. Kim TK, et al. (2010) Widespread transcription at neuronal activity-regulated enhancers. Nature 465(7295):182-187.
23. Blind RD, SuzawaM, Ingraham HA (2012) Direct modification and activation of a nuclear receptor-PIP complex by the inositol lipid kinase IPMK. Sci Signal 5(229):ra44.
24. Endo-Streeter S, Tsui MK, Odom AR, Block J, York JD (2012) Structural studies and protein engineering of inositol phosphate multikinase. J Biol Chem 287(42): 35360-35369.
25. Stevenson-Paulik J, Odom AR, York JD (2002) Molecular and biochemical characterization of two plant inositol polyphosphate 6-/3-/5-kinases. J Biol Chem 277(45): 42711-42718.
26. Alarcón JM, et al. (2004) Chromatin acetylation, memory, and LTP are impaired in CBP+/-mice: A model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 42(6):947-959.
27. Caccamo A, Maldonado MA, Bokov AF, Majumder S, Oddo S (2010) CBP gene transfer increases BDNF levels and ameliorates learning and memory deficits in a mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 107(52):22687-22692.
28. Crump NT, et al. (2011) Dynamic acetylation of all lysine-4 trimethylated histone H3 is evolutionarily conserved and mediated by p300/CBP. Proc Natl Acad Sci USA 108(19): 7814-7819.
29. Giralt A, et al. (2012) Long-term memory deficits in Huntington's disease are associated with reduced CBP histone acetylase activity. Hum Mol Genet 21(6):1203-1216.
30. Korzus E, Rosenfeld MG, Mayford M (2004) CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 42(6):961-972.
31. Petrij F, et al. (1995) Rubinstein-Taybi syndrome caused by mutations in the transcriptional co-activator CBP. Nature 376(6538):348-351.
32. Wang J, et al. (2012) Metformin activates an atypical PKC-CBP pathway to promote neurogenesis and enhance spatial memory formation. Cell Stem Cell 11(1):23-35.
33. Dubois E, Messenguy F (1994) Pleiotropic function of ArgRIIIp (Arg82p), one of the regulators of arginine metabolism in Saccharomyces cerevisiae. Role in expression of cell-type-specific genes. Mol Gen Genet 243(3):315-324.
34. Dubois E, Dewaste V, Erneux C, Messenguy F (2000) Inositol polyphosphate kinase activity of Arg82/ArgRIII is not required for the regulation of the arginine metabolism in yeast. FEBS Lett 486(3):300-304.
35. El Alami M, Messenguy F, Scherens B, Dubois E (2003) Arg82p is a bifunctional protein whose inositol polyphosphate kinase activity is essential for nitrogen and PHO gene expression but not for Mcm1p chaperoning in yeast. Mol Microbiol 49(2):457-468.
36. Odom AR, Stahlberg A, Wente SR, York JD (2000) A role for nuclear inositol 1,4,5-trisphosphate kinase in transcriptional control. Science 287(5460):2026-2029.
37. Bosch D, Saiardi A (2012) Arginine transcriptional response does not require inositol phosphate synthesis. J Biol Chem 287(45):38347-38355.
38. Steger DJ, Haswell ES, Miller AL, Wente SR, O'Shea EK (2003) Regulation of chromatin remodeling by inositol polyphosphates. Science 299(5603):114-116.
39. Watson PJ, Fairall L, Santos GM, Schwabe JW (2012) Structure of HDAC3 bound to co-repressor and inositol tetraphosphate. Nature 481(7381):335-340.
40. Goodman RH, Smolik S (2000) CBP/p300 in cell growth, transformation, and development. Genes Dev 14(13):1553-1577.
41. Ramanan N, et al. (2005) SRF mediates activity-induced gene expression and synaptic plasticity but not neuronal viability. Nat Neurosci 8(6):759-767.
42. Nowak DE, Tian B, Brasier AR (2005) Two-step cross-linking method for identification of NF-kappaB gene network by chromatin immunoprecipitation. Biotechniques 39(5): 715-725.
43. Sunyer B, Patil S, Höger H, Lubec G (October 4, 2007) Barnes maze, a useful task to assess spatial reference memory in the mice. Nature Protocol Exchange, 10.1038/ nprot.2007.390.