Nuclear receptor TLX stimulates hippocampal neurogenesis and enhances learning and memory in a transgenic mouse model

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

Volumn 111, Issue 25, 2014, Pages 9115-9120

  Murai, Kiyohito ^a   Qu, Qiuhao ^a   Sun, GuoQiang ^a   Ye, Peng ^a   Li, Wendong ^a   Asuelime, Grace ^a   Sun, Emily ^a   Tsai, Guochuan E ^b   Shi, Yanhong ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

microRNAs; Neural stem cells; NR2E1

Indexed keywords

CELL NUCLEUS RECEPTOR; MICRORNA; MICRORNA 137; MICRORNA 9; NESTIN; NUCLEAR RECEPTOR TLX; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN WEIGHT; CELL COUNT; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; FOREBRAIN; HIPPOCAMPUS; LEARNING; LONG TERM MEMORY; MEMORY; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHORT TERM MEMORY; SPATIAL MEMORY;

MICRORNAS; NEURAL STEM CELLS; NR2E1;

ANIMALS; COGNITION; DENTATE GYRUS; GENE EXPRESSION; MEMORY; MICE; NESTIN; NEUROGENESIS; NEURONS; PROMOTER REGIONS, GENETIC; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 84903445816     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1406779111     Document Type: Article

References (37)

1. Gage FH (2000) Mammalian neural stem cells. Science 287(5457):1433-1438.
2. Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132(4):645-660. (Pubitemid 351253687)
3. Deng W, Aimone JB, Gage FH (2010) New neurons and new memories: How does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 11(5):339-350.
4. Yu RT, McKeown M, Evans RM, Umesono K (1994) Relationship between Drosophila gap gene tailless and a vertebrate nuclear receptor Tlx. Nature 370(6488):375-379.
5. Monaghan AP, et al. (1997) Defective limbic system in mice lacking the tailless gene. Nature 390(6659):515-517. (Pubitemid 28013132)
6. Shi Y, et al. (2004) Expression and function of orphan nuclear receptor TLX in adult neural stem cells. Nature 427(6969):78-83. (Pubitemid 38094825)
7. Roy K, Thiels E, Monaghan AP (2002) Loss of the tailless gene affects forebrain development and emotional behavior. Physiol Behav 77(4-5):595-600. (Pubitemid 36084407)
8. Young KA, et al. (2002) Fierce: A new mouse deletion of Nr2e1; violent behaviour and ocular abnormalities are background-dependent. Behav Brain Res 132(2):145-158. (Pubitemid 34462042)
9. Sun G, Yu RT, Evans RM, Shi Y (2007) Orphan nuclear receptor TLX recruits histone deacetylases to repress transcription and regulate neural stem cell proliferation. Proc Natl Acad Sci USA 104(39):15282-15287. (Pubitemid 47502909)
10. Sun G, et al. (2010) Histone demethylase LSD1 regulates neural stem cell proliferation. Mol Cell Biol 30(8):1997-2005.
11. Zhao C, Sun G, Li S, Shi Y (2009) A feedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination. Nat Struct Mol Biol 16(4):365-371.
12. Sun G, et al. (2011) miR-137 forms a regulatory loop with nuclear receptor TLX and LSD1 in neural stem cells. Nat Commun 2:529.
13. Zhao C, et al. (2010) MicroRNA let-7b regulates neural stem cell proliferation and differentiation by targeting nuclear receptor TLX signaling. Proc Natl Acad Sci USA 107(5):1876-1881.
14. Zhao C, Sun G, Ye P, Li S, Shi Y (2013) MicroRNA let-7d regulates the TLX/microRNA-9 cascade to control neural cell fate and neurogenesis. Sci Rep 3:1329.
15. Qu Q, et al. (2010) Orphan nuclear receptor TLX activates Wnt/beta-catenin signaling to stimulate neural stem cell proliferation and self-renewal. Nat Cell Biol 12(1):31-39.
16. Zhang CL, Zou Y, He W, Gage FH, Evans RM (2008) A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 451(7181):1004-1007. (Pubitemid 351301727)
17. Liu HK, et al. (2010) The nuclear receptor tailless induces long-term neural stem cell expansion and brain tumor initiation. Genes Dev 24(7):683-695.
18. Roy K, et al. (2004) The Tlx gene regulates the timing of neurogenesis in the cortex. J Neurosci 24(38):8333-8345. (Pubitemid 39280812)
19. Li W, et al. (2008) Nuclear receptor TLX regulates cell cycle progression in neural stem cells of the developing brain. Mol Endocrinol 22(1):56-64.
20. Zimmerman L, et al. (1994) Independent regulatory elements in the nestin gene direct transgene expression to neural stem cells or muscle precursors. Neuron 12(1):11-24. (Pubitemid 24044383)
21. Squire LR (1992) Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychol Rev 99(2):195-231.
22. Deng W, Saxe MD, Gallina IS, Gage FH (2009) Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J Neurosci 29(43):13532-13542.
23. Koch M (1999) The neurobiology of startle. Prog Neurobiol 59(2):107-128.
24. Geyer MA, Swerdlow NR, Mansbach RS, Braff DL (1990) Startle response models of sensorimotor gating and habituation deficits in schizophrenia. Brain Res Bull 25(3):485-498. (Pubitemid 20346586)
25. Geyer MA (2006) Are cross-species measures of sensorimotor gating useful for the discovery of procognitive cotreatments for schizophrenia? Dialogues Clin Neurosci 8(1):9-16.
26. Fenton WS, Stover EL, Insel TR (2003) Breaking the log-jam in treatment development for cognition in schizophrenia: NIMH perspective. Psychopharmacology (Berl) 169(3-4):365-366. (Pubitemid 37255524)
27. Wong BK, et al. (2010) Hyperactivity, startle reactivity and cell-proliferation deficits are resistant to chronic lithium treatment in adult Nr2e1(frc/frc) mice. Genes Brain Behav 9(7):681-694.
28. Snyder JS, Hong NS, McDonald RJ, Wojtowicz JM (2005) A role for adult neurogenesis in spatial long-term memory. Neuroscience 130(4):843-852. (Pubitemid 40094618)
29. Imayoshi I, et al. (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11(10):1153-1161.
30. Jessberger S, et al. (2009) Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem 16(2):147-154.
31. Dupret D, et al. (2008) Spatial relational memory requires hippocampal adult neurogenesis. PLoS ONE 3(4):e1959.
32. Bast T, Feldon J (2003) Hippocampal modulation of sensorimotor processes. Prog Neurobiol 70(4):319-345. (Pubitemid 37107357)
33. Iwata Y, et al. (2008) Irradiation in adulthood as a new model of schizophrenia. PLoS ONE 3(5):e2283.
34. Kumari V, et al. (2008) Uncontrollable voices and their relationship to gating deficits in schizophrenia. Schizophr Res 101(1-3):185-194.
35. Perry W, Minassian A, Feifel D (2004) Prepulse inhibition in patients with non-psychotic major depressive disorder. J Affect Disord 81(2):179-184. (Pubitemid 39070094)
36. Frankland PW, et al. (2004) Sensorimotor gating abnormalities in young males with fragile X syndrome and Fmr1-knockout mice. Mol Psychiatry 9(4):417-425. (Pubitemid 38534702)
37. Kohl S, Heekeren K, Klosterkötter J, Kuhn J (2013) Prepulse inhibition in psychiatric disorders - apart from schizophrenia. J Psychiatr Res 47(4):445-452.