The NR4A orphan nuclear receptors mediate transcription-dependent hippocampal synaptic plasticity

Neurobiology of Learning and Memory

Volumn 105, Issue , 2013, Pages 151-158

  Bridi, Morgan S ^a   Abel, Ted ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

HDAC inhibitor; Hippocampus; Long term potentiation; Nr4a; Nuclear receptors; Synaptic plasticity

Indexed keywords

CELL NUCLEUS RECEPTOR; PROTEIN NR4A; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; LONG TERM MEMORY; LONG TERM POTENTIATION; MALE; MEMORY CONSOLIDATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; NR4A GENE; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSGENE;

HDAC INHIBITOR; HIPPOCAMPUS; LONG-TERM POTENTIATION; NR4A; NUCLEAR RECEPTORS; SYNAPTIC PLASTICITY;

ANIMALS; CA1 REGION, HIPPOCAMPAL; FEMALE; LONG-TERM POTENTIATION; MALE; MICE; MICE, TRANSGENIC; NEURONS; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 1; TRANSCRIPTIONAL ACTIVATION;

EID: 84884203747     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2013.06.020     Document Type: Article

References (51)

1. Abel T., Nguyen P.V., Barad M., Deuel T.A., Kandel E.R., Bourtchouladze R. Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 1997, 88(5):615-626.
2. Abel T., Nguyen P.V. Regulation of hippocampus-dependent memory by cyclic AMP-dependent protein kinase. Progress in Brain Research 2008, 169:97-115.
3. Alberini C.M. Transcription factors in long-term memory and synaptic plasticity. Physiological Reviews 2009, 89(1):121-145.
4. Buervenich S., Carmine A., Arvidsson M., Xiang F., Zhang Z., Sydow O., et al. NURR1 mutations in cases of schizophrenia and manic-depressive disorder. American Journal of Medical Genetics 2000, 96(6):808-813.
5. Chu Y., Kompoliti K., Cochran E.J., Mufson E.J., Kordower J.H. Age-related decreases in Nurr1 immunoreactivity in the human substantia nigra. The Journal of Comparative Neurology 2002, 450(3):203-214.
6. Colón-Cesario W.I., Martínez-Montemayor M.M., Morales S., Félix J., Cruz J., Adorno M., et al. Knockdown of Nurr1 in the rat hippocampus: Implications to spatial discrimination learning and memory. Learning & Memory 2006, 13(6):734-744.
7. Cramer P.E., Cirrito J.R., Wesson D.W., Lee C.Y.D., Karlo J.C., Zinn A.E., et al. ApoE-directed therapeutics rapidly clear β-amyloid and reverse deficits in AD mouse models. Science 2012, 335(6075):1503-1506.
8. Cunha C., Brambilla R., Thomas K.L. A simple role for BDNF in learning and memory?. Frontiers in Molecular Neuroscience 2010, 3(1).
9. Dragunow M., Abraham W., Hughes P. Activation of NMDA and muscarinic receptors induces nur-77 mRNA in hippocampal neurons. Molecular Brain Research 1996, 36:349-356.
10. Dubois C., Hengerer B., Mattes H. Identification of a potent agonist of the orphan nuclear receptor Nurr1. ChemMedChem 2006, 1(9):955-958.
11. Haettig J., Stefanko D.P., Multani M.L., Figueroa D.X., McQuown S.C., Wood M.A. HDAC inhibition modulates hippocampus-dependent long-term memory for object location in a CBP-dependent manner. Learning & Memory 2011, 18:71-79.
12. Hawk J.D., Abel T. The role of NR4A transcription factors in memory formation. Brain Research Bulletin 2011, 85(1-2):21-29.
13. Hawk J.D., Bookout A.L., Poplawski S.G., Bridi M., Rao A.J., Sulewski M.E., et al. NR4A nuclear receptors support memory enhancement by histone deacetylase inhibitors. The Journal of Clinical Investigation 2012, 122(10):3593-3602.
14. Huang Y., Kandel E.R. Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippocampus requires repeated tetanization. Learning & Memory 1994, 1(1):74-82.
15. Huang Y.Y., Nguyen P.V., Abel T., Kandel E.R. Long-lasting forms of synaptic potentiation in the mammalian hippocampus. Learning & Memory 1996, 3(2-3):74-85.
16. Igaz L.M., Vianna M.R.M., Medina J.H., Izquierdo I. Two time periods of hippocampal mRNA synthesis are required for memory consolidation of fear-motivated learning. The Journal of Neuroscience 2002, 22(15):6781-6789.
17. Inamoto T., Papineni S., Chintharlapalli S., Cho S.-D., Safe S., Kamat A.M. 1,1-Bis(3'-indolyl)-1-(p-chlorophenyl)methane activates the orphan nuclear receptor Nurr1 and inhibits bladder cancer growth. Molecular Cancer Therapeutics 2008, 7(12):3825-3833.
18. Jiang Q., Lee C.Y.D., Mandrekar S., Wilkinson B., Cramer P., Zelcer N., et al. ApoE promotes the proteolytic degradation of Abeta. Neuron 2008, 58(5):681-693.
19. Johnson M.M., Michelhaugh S.K., Bouhamdan M., Schmidt C.J., Bannon M.J. The transcription factor NURR1 exerts concentration-dependent effects on target genes mediating distinct biological processes. Frontiers in Neuroscience 2011, 5:135.
20. Josselyn S.A., Nguyen P.V. CREB, synapes, and memory disorders: Past progress and future challenges. Current Drug Targets - CNS & Neurological Disorders 2005, 4(5):481-497.
21. Kovalovsky D., Refojo D., Liberman A.C., Hochbaum D., Pereda M.P., Coso O.A., et al. Activation and induction of NUR77/NURR1 in corticotrophs by CRh/cAMP: Involvement of calcium, protein kinase A, and MAPK pathways. Molecular Endocrinology 2002, 16(7):1638-1651.
22. Lattal K.M., Barrett R.M., Wood M.A. Systemic or intrahippocampal delivery of histone deacetylase inhibitors facilitates fear extinction. Behavioral Neuroscience 2007, 121(5):1125-1131.
23. Lemberger T., Parkitna J.R., Chai M., Schütz G., Engblom D. CREB has a context-dependent role in activity-regulated transcription and maintains neuronal cholesterol homeostasis. The FASEB Journal 2008, 22(8):2872-2879.
24. Levenson J.M., O'Riordan K.J., Brown K.D., Trinh M.A., Molfese D.L., Sweatt J.D. Regulation of histone acetylation during memory formation in the hippocampus. The Journal of Biological Chemistry 2004, 279(39):40545-40559.
25. Li X., Lee S.-O., Safe S. Structure-dependent activation of NR4A2 (Nurr1) by 1,1-bis(3'-indolyl)-1-(aromatic)methane analogs in pancreatic cancer cells. Biochemical Pharmacology 2012, 83(10):1445-1455.
26. Mangelsdorf D.J., Evans R.M. The RXR heterodimers and orphan receptors. Cell 1995, 83(6):841-850.
27. Martin S.J., Grimwood P.D., Morris R.G.M. Synaptic plasticity and memory: An evaluation of the hypothesis. Annual Review of Neuroscience 2000, 23:649-711.
28. Maxwell M., Muscat G.E.O. The NR4A subgroup: Immediate early response genes with pleiotropic physiological roles. Nuclear Receptor Signaling 2006, 4:e002.
29. Mayford M., Bach M.E., Huang Y.Y., Wang L., Hawkins R.D., Kandel E.R. Control of memory formation through regulated expression of a CaMKII transgene. Science 1996, 274(5293):1678-1683.
30. McNulty S.E., Barrett R.M., Vogel-Ciernia A., Malvaez M., Hernandez N., Davatolhagh M.F., et al. Differential roles for Nr4a1 and Nr4a2 in object location vs. object recognition long-term memory. Learning & Memory 2012, 19(12):588-592.
31. McQuown S.C., Barrett R.M., Matheos D.P., Post R.J., Rogge G.A., Alenghat T., et al. HDAC3 is a critical negative regulator of long-term memory formation. The Journal of Neuroscience 2011, 31(2):764-774.
32. Nguyen P.V., Abel T., Kandel E.R. Requirement of a critical period of transcription for induction of a late phase of LTP. Science 1994, 265(5175):1104-1107.
33. Nguyen P.V., Kandel E.R. Brief theta-burst stimulation induces a transcription-dependent late phase of LTP requiring cAMP in area CA1 of the mouse hippocampus. Learning & Memory 1997, 4(2):230-243.
34. Paulsen R.E., Weaver C.A., Fahrner T.J., Milbrandt J. Domains regulating transcriptional activity of the inducible orphan receptor NGFI-B. The Journal of Biological Chemistry 1992, 267(23):16491-19496.
35. Pedersen W.A., McMillan P.J., Kulstad J.J., Leverenz J.B., Craft S., Haynatzki G.R. Rosiglitazone attenuates learning and memory deficits in Tg2576 Alzheimer mice. Experimental Neurology 2006, 199(2):265-273.
36. Pegoraro S., Broccard F.D., Ruaro M.E., Bianchini D., Avossa D., Pastore G., et al. Sequential steps underlying neuronal plasticity induced by a transient exposure to gabazine. The Journal of Cellular Physiology 2010, 222:713-728.
37. Peña de Ortiz S., Jamieson G.A. HZF-3, an immediate-early orphan receptor homologous to NURR1/NOT: Induction upon membrane depolarization and seizures. Molecular Brain Research 1996, 38(1):1-13.
38. Peña de Ortiz S., Maldonado-Vlaar C.S., Carrasquillo Y. Hippocampal expression of the orphan nuclear receptor gene hzf-3/nurr1 during spatial discrimination learning. Neurobiology of Learning and Memory 2000, 74(2).
39. Pittenger C., Huang Y.Y., Paletzki R.F., Bourtchouladze R., Scanlin H., Vronskaya S., et al. Reversible inhibition of CREB/ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampus-dependent spatial memory. Neuron 2002, 34(3):447-462.
40. Robert N.M., Martin L.J., Tremblay J.J. The orphan nuclear receptor NR4A1 regulates insulin-like 3 gene transcription in Leydig cells. Biology of Reproduction 2006, 74(2):322-330.
41. Rojas P., Joodmardi E., Hong Y., Perlmann T., Ogren S.O. Adult mice with reduced Nurr1 expression: An animal model for schizophrenia. Molecular Psychiatry 2007, 12(8):756-766.
42. Ryan M.M., Mason-Parker S.E., Tate W.P., Abraham W.C., Williams J.M. Rapidly induced gene networks following induction of long-term potentiation at perforant path synapses in vivo. Hippocampus 2011, 21:541-553.
43. Stafford J.M., Raybuck J.D., Ryabinin A.E., Lattal K.M. Increasing histone acetylation in the hippocampus-infralimbic network enhances fear extinction. Biological Psychiatry 2012, 72(1):25-33.
44. Stefanko D.P., Barrett R.M., Ly A.R., Reolon G.K., Wood M.A. Modulation of long-term memory for object recognition via HDAC inhibition. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(23):9447-9452.
45. Vecsey C.G., Baillie G.S., Jaganath D., Havekes R., Daniels A., Wimmer M., et al. Sleep deprivation impairs cAMP signalling in the hippocampus. Nature 2009, 461(7267):1122-1125.
46. Vecsey C.G., Hawk J.D., Lattal K.M., Stein J.M., Fabian S.A., Attner M.A., et al. Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. The Journal of Neuroscience 2007, 27(23):6128-6140.
47. Volpicelli F., Caiazzo M., Greco D., Consales C., Leone L., Perrone-Capano C., et al. Bdnf gene is a downstream target of Nurr1 transcription factor in rat midbrain neurons in vitro. Journal of Neurochemistry 2007, 102(2):441-453.
48. Von Hertzen L.S.J., Giese K.P. Memory reconsolidation engages only a subset of immediate-early genes induced during consolidation. The Journal of Neuroscience 2005, 25(8):1935-1942.
49. Wansa K.D.S.A., Harris J.M., Yan G., Ordentlich P., Muscat G.E.O. The AF-1 domain of the orphan nuclear receptor NOR-1 mediates trans-activation, coactivator recruitment, and activation by the purine anti-metabolite 6-mercaptopurine. The Journal of Biological Chemistry 2003, 278:24776-24790.
50. Wesson D.W., Borkowski A.H., Landreth G.E., Nixon R.A., Levy E. Sensory network dysfunction, behavioral impairments, and their reversibility in an Alzheimer's β-amyloidosis mouse model. The Journal of Neuroscience 2011, 31(44):15962-15971.
51. Xing G., Zhang L., Russell S., Post R. Reduction of dopamine-related transcription factors Nurr1 and NGFI-B in the prefrontal cortex in schizophrenia and bipolar disorders. Schizophrenia Research 2006, 84(1):36-56.