Norepinephrine directly activates adult hippocampal precursors via β3-adrenergic receptors

Journal of Neuroscience

Volumn 30, Issue 7, 2010, Pages 2795-2806

  Jhaveri, Dhanisha J ^a   Mackay, Eirinn W ^a   Hamlin, Adam S ^a   Marathe, Swananda V ^c   Nandam, L Sanjay ^a,b   Vaidya, Vidita A ^c   Bartlett, Perry F ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b THE PRINCE CHARLES HOSPITAL   (Australia)

^c TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 3 ADRENERGIC RECEPTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; ISOPRENALINE; NESTIN; NORADRENALIN; SEROTONIN; TRANSCRIPTION FACTOR HES 5;

ANIMAL TISSUE; ARTICLE; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; HIPPOCAMPUS; MALE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL;

ADRENERGIC AGONISTS; ADRENERGIC ALPHA-AGONISTS; ADRENERGIC ANTAGONISTS; ADULT STEM CELLS; ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; FLOW CYTOMETRY; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYELIN BASIC PROTEINS; NOREPINEPHRINE; RATS; RATS, WISTAR; RECEPTORS, ADRENERGIC, BETA-3; STATISTICS, NONPARAMETRIC; TUBULIN;

EID: 77249102054     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3780-09.2010     Document Type: Article

References (54)

1. Basak O, Taylor V (2007) Identification of self-replicating multipotent progenitors in the embryonic nervous system by high Notch activity and Hes5 expression. Eur J Neurosci 25:1006-1022.
2. Brezun JM, Daszuta A (1999) Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats. Neuroscience 89:999-1002.
3. Brezun JM, Daszuta A (2000) Serotonergic reinnervation reverses lesioninduced decreases in PSA-NCAM labeling and proliferation of hippocampal cells in adult rats. Hippocampus 10:37-46.
4. Bull ND, Bartlett PF (2005) The adult mouse hippocampal progenitor is neurogenic but not a stem cell. J Neurosci 25:10815-10821.
5. Charney DS (1998) Monoamine dysfunction and the pathophysiology and treatment of depression. J Clin Psychiatry 59 [Suppl 14]:11-14.
6. Cikos S, Veselá J, Il'ková G, Rehák P, Czikková S, Koppel J (2005) Expression of β adrenergic receptors in mouse oocytes and preimplantation embryos. Mol Reprod Dev 71:145-153.
7. Claustre Y, Leonetti M, Santucci V, Bougault I, Desvignes C, Rouquier L, Aubin N, Keane P, Busch S, Chen Y, Palejwala V, Tocci M, Yamdagni P, Didier M, Avenet P, Le Fur G, Oury-Donat F, Scatton B, Steinberg R (2008) Effects of the β3-adrenoceptor (Adrb3) agonist SR58611A (amibegron) on serotonergic and noradrenergic transmission in the rodent: relevance to its antidepressant/ anxiolytic-like profile. Neuroscience 156:353-364.
8. Consoli D, Leggio GM, Mazzola C, Micale V, Drago F (2007) Behavioral effects of the β3 adrenoceptor agonist SR58611A: is it the putative prototype of a new class of antidepressant/anxiolytic drugs? Eur J Pharmacol 573:139-147.
9. Couillard-Despres S, Wuertinger C, Kandasamy M, Caioni M, Stadler K, Aigner R, Bogdahn U, Aigner L (2009) Ageing abolishes the effects of fluoxetine on neurogenesis. Mol Psychiatry 14:856-864.
10. Cryan JF, O'Leary OF, Jin SH, Friedland JC, Ouyang M, Hirsch BR, Page ME, Dalvi A, Thomas SA, Lucki I (2004) Norepinephrine-deficient mice lack responses to antidepressant drugs, including selective serotonin reuptake inhibitors. Proc Natl Acad Sci U S A 101:8186-8191.
11. David DJ, Samuels BA, Rainer Q, Wang JW, Marsteller D, Mendez I, Drew M, Craig DA, Guiard BP, Guilloux JP, Artymyshyn RP, Gardier AM, Gerald C, Antonijevic IA, Leonardo ED, Hen R (2009) Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/ depression. Neuron 62:479-493.
12. Deisseroth K, Singla S, Toda H, Monje M, Palmer TD, Malenka RC (2004) Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42:535-552.
13. Encinas JM, Vaahtokari A, Enikolopov G (2006) Fluoxetine targets early progenitor cells in the adult brain. Proc Natl Acad Sci U S A 103:8233-8238.
14. Evans BA, Papaioannou M, Hamilton S, Summers RJ (1999) Alternative splicing generates two isoforms of the β3-adrenoceptor which are differentially expressed in mouse tissues. Br J Pharmacol 127:1525-1531.
15. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439:589-593.
16. Ge S, Pradhan DA, Ming GL, Song H (2007) GABA sets the tempo for activity-dependent adult neurogenesis. Trends Neurosci 30:1-8.
17. Gould E (1999) Serotonin and hippocampal neurogenesis. Neuropsychopharmacology 21:46S-51S.
18. Hagg T (2009) From neurotransmitters to neurotrophic factors to neurogenesis. Neuroscientist 15:20-27.
19. Holick KA, Lee DC, Hen R, Dulawa SC (2008) Behavioral effects of chronic fluoxetine in BALB/cJ mice do not require adult hippocampal neurogenesis or the serotonin 1A receptor. Neuropsychopharmacology 33:406-417.
20. Huang GJ, Herbert J (2006) Stimulation of neurogenesis in the hippocampus of the adult rat by fluoxetine requires rhythmic change in corticosterone. Biol Psychiatry 59:619-624.
21. Huang GJ, Bannerman D, Flint J (2008) Chronic fluoxetine treatment alters behavior, but not adult hippocampal neurogenesis, in BALB/cJ mice. Mol Psychiatry 13:119-121.
22. Hyttel J (1994) Pharmacological characterization of selective serotonin reuptake inhibitors (SSRIs). Int Clin Psychopharmacol 9 [Suppl 1]:19-26.
23. Jha S, Rajendran R, Davda J, Vaidya VA (2006) Selective serotonin depletion does not regulate hippocampal neurogenesis in the adult rat brain: differential effects of p-chlorophenylalanine and 5,7- dihydroxytryptamine. Brain Res 1075:48-59.
24. Kageyama R, Ohtsuka T, Hatakeyama J, Ohsawa R (2005) Roles of bHLH genes in neural stem cell differentiation. Exp Cell Res 306:343-348.
25. Kempermann G, Jessberger S, Steiner B, Kronenberg G (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27:447-452.
26. Kulkarni VA, Jha S, Vaidya VA (2002) Depletion of norepinephrine decreases the proliferation, but does not influence the survival and differentiation, of granule cell progenitors in the adult rat hippocampus. Eur J Neurosci 16:2008-2012.
27. Lacaille JC, Harley CW (1985) The action of norepinephrine in the dentate gyrus: β-mediated facilitation of evoked potentials in vitro. Brain Res 358:210-220.
28. Lledo PM, Alonso M, Grubb MS (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7:179-193.
29. Ma DK, Jang MH, Guo JU, Kitabatake Y, Chang ML, Pow-Anpongkul N, Flavell RA, Lu B, Ming GL, Song H (2009) Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323:1074-1077.
30. Malberg JE, Duman RS (2003) Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 28:1562-1571.
31. Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20:9104-9110.
32. Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223-250.
33. Nácher J, Varea E, Miguel Blasco-Ibáñez J, Gómez-Climent MA, Castillo-Gómez E, Crespo C, Martínez- Guijarro FJ, McEwen BS (2007) N-Methyl-D-aspartate receptor expression during adult neurogenesis in the rat dentate gyrus. Neuroscience 144:855-864.
34. Nakagawa S, Kim JE, Lee R, Malberg JE, Chen J, Steffen C, Zhang YJ, Nestler EJ, Duman RS (2002) Regulation of neurogenesis in adult mouse hippocampus by cAMP and the cAMP response element-binding protein. J Neurosci 22:3673-3682.
35. Ohtsuka T, Imayoshi I, Shimojo H, Nishi E, Kageyama R, McConnell SK (2006) Visualization of embryonic neural stem cells using Hes promoters in transgenic mice. Mol Cell Neurosci 31:109 -122.
36. Ozawa H, Otsuki I, Shiroishi Y (1969) Supersensitivity to isoproterenol and a new adrenergic β-mimetic agent trimethoquinol on the blood pressure of the reserpine treated rat. Jpn J Pharmacol 19:110 -114.
37. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, Ed 2. London: Academic.
38. 2-adrenoceptor antagonist dexefaroxan enhances hippocampal neurogenesis by increasing the survival and differentiation of new granule cells. Neuropsychopharmacology 31:1146-1157.
39. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:805-809.
40. Segal M (1980) The action of serotonin in the rat hippocampal slice preparation. J Physiol 303:423-439.
41. Simiand J, Keane PE, Guitard J, Langlois X, Gonalons N, Martin P, Bianchetti A, Le Fur G, Soubrié P (1992) Antidepressant profile in rodents of SR 58611A, a new selective agonist for atypical β-adrenoceptors. Eur J Pharmacol 219:193-201.
42. Stemmelin J, Cohen C, Terranova JP, Lopez-Grancha M, Pichat P, Bergis O, Decobert M, Santucci V, FrançonD, Alonso R, Stahl SM, Keane P, Avenet P, Scatton B, le Fur G, Griebel G (2008) Stimulation of the β3-adrenoceptor as a novel treatment strategy for anxiety and depressive disorders. Neuropsychopharmacology 33:574-587.
43. Strosberg AD (1997) Association of β3-adrenoceptor polymorphism with obesity and diabetes: current status. Trends Pharmacol Sci 18:449-454.
44. Summers RJ, Papaioannou M, Harris S, Evans BA (1995) Expression of β3-adrenoceptor mRNA in rat brain. Br J Pharmacol 116:2547-2548.
45. Tashiro A, Sandler VM, Toni N, Zhao C, Gage FH (2006) NMDA-receptormediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 442:929-933.
46. Ursino MG, Vasina V, Raschi E, Crema F, De Ponti F (2009) The β3-adrenoceptor as a therapeutic target: current perspectives. Pharmacol Res 59:221-234.
47. Vaidya VA, Vadodaria KC, Jha S (2007) Neurotransmitter regulation of adult neurogenesis: putative therapeutic targets. CNS Neurol Disord Drug Targets 6:358-374.
48. Vollmayr B, Mahlstedt MM, Henn FA (2007) Neurogenesis and depression: what animal models tell us about the link. Eur Arch Psychiatry Clin Neurosci 257:300-303.
49. Walker TL, White A, Black DM, Wallace RH, Sah P, Bartlett PF (2008) Latent stem and progenitor cells in the hippocampus are activated by neural excitation. J Neurosci 28:5240-5247.
50. Wang JW, David DJ, Monckton JE, Battaglia F, Hen R (2008) Chronic fluoxetine stimulates maturation and synaptic plasticity of adult-born hippocampal granule cells. J Neurosci 28:1374-1384.
51. 2-Adrenoceptor blockade accelerates the neurogenic, neurotrophic, and behavioral effects of chronic antidepressant treatment. J Neurosci 30:1096-1109.
52. Yu TS, Dandekar M, Monteggia LM, Parada LF, Kernie SG (2005) Temporally regulated expression of Cre recombinase in neural stem cells. Genesis 41:147-153.
53. Yuan Q, Harley CW, Bruce JC, Darby-King A, McLean JH (2000) Isoproterenol increases CREB phosphorylation and olfactory nerve-evoked potentials in normal and 5-HT-depleted olfactory bulbs in rat pups only at doses that produce odor preference learning. Learn Mem 7:413-421.
54. Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132:645-660.