The nuclear receptor REV-ERBα regulates Fabp7 and modulates adult hippocampal neurogenesis

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Schnell, Anna ^a   Chappuis, Sylvie ^a,d   Schmutz, Isabelle ^a,e   Brai, Emanuele ^a   Ripperger, Jürgen A ^a   Schaad, Olivier ^b   Welzl, Hans ^c   Descombes, Patrick ^b,f   Alberi, Lavinia ^a   Albrecht, Urs ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d Vifor (International) Inc   (Switzerland)

^e ROCKEFELLER UNIVERSITY   (United States)

^f NESTLÉ RESEARCH CENTER   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID BINDING PROTEIN; FATTY ACID BINDING PROTEIN 7; MESSENGER RNA; NUCLEAR RECEPTOR NR1D1; UNCLASSIFIED DRUG; CARRIER PROTEIN; FABP7 PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN;

ADULT; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BRAIN REGION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION; GENETIC ASSOCIATION; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; MALE; MOLECULAR DYNAMICS; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; RNA SEQUENCE; SEQUENCE ANALYSIS; AFFECT; AGING; ANIMAL; CELL MOTION; CIRCADIAN RHYTHM; COGNITION; DEFICIENCY; DENTATE GYRUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOME; GLIOBLASTOMA; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROMOTER REGION; TUMOR CELL LINE;

AFFECT; AGING; ANIMALS; BEHAVIOR, ANIMAL; CARRIER PROTEINS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CIRCADIAN RHYTHM; COGNITION; DENTATE GYRUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOME; GLIOBLASTOMA; HIPPOCAMPUS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE, KNOCKOUT; NEUROGENESIS; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP D, MEMBER 1; PROMOTER REGIONS, GENETIC; RATS; RNA, MESSENGER; TUMOR SUPPRESSOR PROTEINS;

EID: 84903177583     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099883     Document Type: Article

References (68)

1. Buhr ED, Takahashi JS (2013) Molecular components of the Mammalian circadian clock. Handb Exp Pharmacol 217: 3-27.
2. Bugge A, Feng D, Everett LJ, Briggs ER, Mullican SE, et al. (2012) Reverbalpha and Rev-erbbeta coordinately protect the circadian clock and normal metabolic function. Genes Dev 26: 657-667.
3. Cho H, Zhao X, Hatori M, Yu RT, Barish GD, et al. (2012) Regulation of circadian behaviour and metabolism by REV-ERB-alpha and REV-ERB-beta. Nature 485: 123-127.
4. Solt LA, Wang Y, Banerjee S, Hughes T, Kojetin DJ, et al. (2012) Regulation of circadian behaviour and metabolism by synthetic REV-ERB agonists. Nature 485: 62-68.
5. Borgs L, Beukelaers P, Vandenbosch R, Nguyen L, Moonen G, et al. (2009) Period 2 regulates neural stem/progenitor cell proliferation in the adult hippocampus. BMC Neurosci 10: 30.
6. Kimiwada T, Sakurai M, Ohashi H, Aoki S, Tominaga T, et al. (2009) Clock genes regulate neurogenic transcription factors, including NeuroD1, and the neuronal differentiation of adult neural stem/progenitor cells. Neurochem Int 54: 277-285.
7. Bracko O, Singer T, Aigner S, Knobloch M, Winner B, et al. (2012) Gene expression profiling of neural stem cells and their neuronal progeny reveals IGF2 as a regulator of adult hippocampal neurogenesis. J Neurosci 32: 3376-3387.
8. Janich P, Pascual G, Merlos-Suarez A, Batlle E, Ripperger J, et al. (2011) The circadian molecular clock creates epidermal stem cell heterogeneity. Nature 480: 209-214.
9. Janich P, Toufighi K, Solanas G, Luis NM, Minkwitz S, et al. (2013) Human epidermal stem cell function is regulated by circadian oscillations. Cell Stem Cell 13: 745-753.
10. Lie DC, Song H, Colamarino SA, Ming GL, Gage FH (2004) Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annu Rev Pharmacol Toxicol 44: 399-421. (Pubitemid 38263847)
11. Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132: 645-660. (Pubitemid 351253687)
12. Samuels BA, Hen R (2011) Neurogenesis and affective disorders. Eur J Neurosci 33: 1152-1159.
13. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264: 1145-1148. (Pubitemid 24210676)
14. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16: 2027-2033. (Pubitemid 26144015)
15. Gould E, McEwen BS, Tanapat P, Galea LA, Fuchs E (1997) Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 17: 2492-2498. (Pubitemid 27137415)
16. Gould E, Tanapat P, Cameron HA (1997) Adrenal steroids suppress granule cell death in the developing dentate gyrus through an NMDA receptor-dependent mechanism. Brain Res Dev Brain Res 103: 91-93. (Pubitemid 27465714)
17. van Praag H, Kempermann G, Gage FH (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2: 266-270. (Pubitemid 30491298)
18. Guzman-Marin R, Suntsova N, Stewart DR, Gong H, Szymusiak R, et al. (2003) Sleep deprivation reduces proliferation of cells in the dentate gyrus of the hippocampus in rats. J Physiol 549: 563-571. (Pubitemid 36701766)
19. Kempermann G, Kuhn HG, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386: 493-495. (Pubitemid 27164074)
20. Gibson EM, Wang C, Tjho S, Khattar N, Kriegsfeld LJ (2010) Experimental 'jet lag' inhibits adult neurogenesis and produces long-term cognitive deficits in female hamsters. PLoS One 5: e15267.
21. Kott J, Leach G, Yan L (2012) Direction-dependent effects of chronic "jet-lag" on hippocampal neurogenesis. Neurosci Lett 515: 177-180.
22. Golombek DA, Rosenstein RE (2010) Physiology of circadian entrainment. Physiol Rev 90: 1063-1102.
23. Goergen EM, Bagay LA, Rehm K, Benton JL, Beltz BS (2002) Circadian control of neurogenesis. J Neurobiol 53: 90-95.
24. Kochman LJ, Weber ET, Fornal CA, Jacobs BL (2006) Circadian variation in mouse hippocampal cell proliferation. Neurosci Lett 406: 256-259. (Pubitemid 44322025)
25. Tamai S, Sanada K, Fukada Y (2008) Time-of-day-dependent enhancement of adult neurogenesis in the hippocampus. PLoS One 3: e3835.
26. Gilhooley MJ, Pinnock SB, Herbert J (2011) Rhythmic expression of per1 in the dentate gyrus is suppressed by corticosterone: implications for neurogenesis. Neurosci Lett 489: 177-181.
27. Preitner N, Damiola F, Lopez-Molina L, Zakany J, Duboule D, et al. (2002) The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110: 251-260. (Pubitemid 34876552)
28. Chmurzynska A (2006) The multigene family of fatty acid-binding proteins (FABPs): function, structure and polymorphism. J Appl Genet 47: 39-48.
29. Feng L, Hatten ME, Heintz N (1994) Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron 12: 895-908. (Pubitemid 24126249)
30. Yun SW, Leong C, Zhai D, Tan YL, Lim L, et al. (2012) Neural stem cell specific fluorescent chemical probe binding to FABP7. Proc Natl Acad Sci U S A 109: 10214-10217.
31. Young JK, Heinbockel T, Gondre-Lewis MC (2013) Astrocyte fatty acid binding protein-7 is a marker for neurogenic niches in the rat hippocampus. Hippocampus 23: 1476-1483.
32. Giachino C, Basak O, Lugert S, Knuckles P, Obernier K, et al. (2014) Molecular diversity subdivides the adult forebrain neural stem cell population. Stem Cells 32: 70-84.
33. Gerstner JR, Bremer QZ, Vander Heyden WM, Lavaute TM, Yin JC, et al. (2008) Brain fatty acid binding protein (Fabp7) is diurnally regulated in astrocytes and hippocampal granule cell precursors in adult rodent brain. PLoS One 3: e1631.
34. Gerstner JR, Vanderheyden WM, LaVaute T, Westmark CJ, Rouhana L, et al. (2012) Time of day regulates subcellular trafficking, tripartite synaptic localization, and polyadenylation of the astrocytic Fabp7 mRNA. J Neurosci 32: 1383-1394.
35. Hamprecht B (1977) Structural, electrophysiological, biochemical, and pharmacological properties of neuroblastoma-glioma cell hybrids in cell culture. Int Rev Cytol 49: 99-170.
36. Ponten J, Westermark B (1978) Properties of human malignant glioma cells in vitro. Med Biol 56: 184-193. (Pubitemid 9039998)
37. Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193. (Pubitemid 36181903)
38. Albrecht U, Sun ZS, Eichele G, Lee CC (1997) A differential response of two putative mammalian circadian regulators, mper1 and mper2, to light. Cell 91: 1055-1064. (Pubitemid 28027837)
39. Schmutz I, Ripperger JA, Baeriswyl-Aebischer S, Albrecht U (2010) The mammalian clock component PERIOD2 coordinates circadian output by interaction with nuclear receptors. Genes Dev 24: 345-357.
40. Langmesser S, Tallone T, Bordon A, Rusconi S, Albrecht U (2008) Interaction of circadian clock proteins PER2 and CRY with BMAL1 and CLOCK. BMC Mol Biol 9: 41.
41. Ripperger JA, Schibler U (2006) Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions. Nat Genet 38: 369-374.
42. Stratmann M, Stadler F, Tamanini F, van der Horst GT, Ripperger JA (2010) Flexible phase adjustment of circadian albumin D site-binding protein (DBP) gene expression by CRYPTOCHROME1. Genes Dev 24: 1317-1328.
43. Braff DL, Geyer MA (1990) Sensorimotor gating and schizophrenia. Human and animal model studies. Arch Gen Psychiatry 47: 181-188. (Pubitemid 20058094)
44. Reppert SM, Weaver DR (2002) Coordination of circadian timing in mammals. Nature 418: 935-941. (Pubitemid 34976023)
45. Crumbley C, Burris TP (2011) Direct regulation of CLOCK expression by REV-ERB. PLoS One 6: e17290.
46. Watanabe A, Toyota T, Owada Y, Hayashi T, Iwayama Y, et al. (2007) Fabp7 maps to a quantitative trait locus for a schizophrenia endophenotype. PLoS Biol 5: e297.
47. Hampp G, Ripperger JA, Houben T, Schmutz I, Blex C, et al. (2008) Regulation of monoamine oxidase A by circadian-clock components implies clock influence on mood. Curr Biol 18: 678-683.
48. Petit-Demouliere B, Chenu F, Bourin M (2005) Forced swimming test in mice: a review of antidepressant activity. Psychopharmacology (Berl) 177: 245-255. (Pubitemid 40137284)
49. Renard CE, Dailly E, David DJ, Hascoet M, Bourin M (2003) Monoamine metabolism changes following the mouse forced swimming test but not the tail suspension test. Fundam Clin Pharmacol 17: 449-455. (Pubitemid 36920646)
50. Lalonde R (2002) The neurobiological basis of spontaneous alternation. Neurosci Biobehav Rev 26: 91-104.
51. Wimmer ME, Hernandez PJ, Blackwell J, Abel T (2012) Aging impairs hippocampus-dependent long-term memory for object location in mice. Neurobiol Aging 33: 2220-2224.
52. Jager J, O'Brien WT, Manlove J, Krizman EN, Fang B, et al. (2014) Behavioral Changes and Dopaminergic Dysregulation in Mice Lacking the Nuclear Receptor Rev-erbalpha. Mol Endocrinol 28: 490-498.
53. Snyder JS, Soumier A, Brewer M, Pickel J, Cameron HA (2011) Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 476: 458-461.
54. Owada Y, Abdelwahab SA, Kitanaka N, Sakagami H, Takano H, et al. (2006) Altered emotional behavioral responses in mice lacking brain-type fatty acidbinding protein gene. Eur J Neurosci 24: 175-187. (Pubitemid 44050677)
55. Gu Y, Janoschka S, Ge S (2013) Neurogenesis and hippocampal plasticity in adult brain. Curr Top Behav Neurosci 15: 31-48.
56. Kojetin D, Wang Y, Kamenecka TM, Burris TP (2011) Identification of SR8278, a synthetic antagonist of the nuclear heme receptor REV-ERB. ACS Chem Biol 6: 131-134.
57. De Rosa A, Pellegatta S, Rossi M, Tunici P, Magnoni L, et al. (2012) A radial glia gene marker, fatty acid binding protein 7 (FABP7), is involved in proliferation and invasion of glioblastoma cells. PLoS One 7: e52113.
58. Mu Y, Gage FH (2011) Adult hippocampal neurogenesis and its role in Alzheimer's disease. Mol Neurodegener 6: 85.
59. Bizon JL, Helm KA, Han JS, Chun HJ, Pucilowska J, et al. (2001) Hypothalamic-pituitary-adrenal axis function and corticosterone receptor expression in behaviourally characterized young and aged Long-Evans rats. Eur J Neurosci 14: 1739-1751. (Pubitemid 35478042)
60. Lee SY, Hwang YK, Yun HS, Han JS (2012) Decreased levels of nuclear glucocorticoid receptor protein in the hippocampus of aged Long-Evans rats with cognitive impairment. Brain Res 1478: 48-54.
61. Akers KG, Martinez-Canabal A, Restivo L, Yiu AP, De Cristofaro A, et al. (2014) Hippocampal neurogenesis regulates forgetting during adulthood and infancy. Science 344: 598-602.
62. Basak O, Giachino C, Fiorini E, Macdonald HR, Taylor V (2012) Neurogenic subventricular zone stem/progenitor cells are Notch1-dependent in their active but not quiescent state. J Neurosci 32: 5654-5666.
63. Chomez P, Neveu I, Mansen A, Kiesler E, Larsson L, et al. (2000) Increased cell death and delayed development in the cerebellum of mice lacking the reverbA (alpha) orphan receptor. Development 127: 1489-1498. (Pubitemid 30232599)
64. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, et al. (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63: 5821-5828. (Pubitemid 37187480)
65. Alcantara Llaguno, Chen J, Parada LF (2009) Signaling in malignant astrocytomas: role of neural stem cells and its therapeutic implications. Clin Cancer Res 15: 7124-7129.
66. Madden MH, Anic GM, Thompson RC, Nabors LB, Olson JJ, et al. (2014) Circadian pathway genes in relation to glioma risk and outcome. Cancer Causes Control 25: 25-32.
67. Li A, Lin X, Tan X, Yin B, Han W, et al. (2013) Circadian gene Clock contributes to cell proliferation and migration of glioma and is directly regulated by tumor-suppressive miR-124. FEBS Lett 587: 2455-2460.
68. Encinas JM, Michurina TV, Peunova N, Park JH, Tordo J, et al. (2011) Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell 8: 566-579.