GluN2B-containg NMDA receptors on adult-born granule cells contribute to the antidepressant action of fluoxetine

Frontiers in Neuroscience

Volumn 10, Issue MAY, 2016, Pages

  Tannenholz, Lindsay ^a,b   Hen, René ^a,b   Kheirbek, Mazen A ^a,b,c  

^a Howard Hughes Medical Institute   (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Antidepressants; Dentate gyrus granule cells; GluN2B; Neurogenesis; Selective serotonin reuptake inhibitor (SSRI); Synaptic plasticity

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B;

ADULT; ANALYSIS OF VARIANCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; EXON; GENETIC RECOMBINATION; GRANULE CELL; HEMIZYGOSITY; HIPPOCAMPUS; HOMOZYGOSITY; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN EXPRESSION;

EID: 84973526862     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2016.00242     Document Type: Article

References (82)

1. Airan, R. D., Meltzer, L. A., Roy, M., Gong, Y., Chen, H., and Deisseroth, K. (2007). High-speed imaging reveals neurophysiological links to behavior in an animal model of depression. Science 317, 819-823. doi: 10.1126/science.1144400
2. Baek, I. S., Park, J. Y., and Han, P. L. (2015). Chronic antidepressant treatment in normal mice induces anxiety and impairs stress-coping ability. Exp. Neurobiol. 24, 156-168. doi: 10.5607/en.2015.24.2.156
3. Bergami, M., Rimondini, R., Santi, S., Blum, R., Gotz, M., and Canossa, M. (2008). Deletion of TrkB in adult progenitors alters newborn neuron integration into hippocampal circuits and increases anxiety-like behavior. Proc. Natl. Acad. Sci. U.S.A. 105, 15570-15575. doi: 10.1073/pnas.0803702105
4. Bondi, C. O., Rodriguez, G., Gould, G. G., Frazer, A., and Morilak, D. A. (2008). Chronic unpredictable stress induces a cognitive deficit and anxiety-like behavior in rats that is prevented by chronic antidepressant drug treatment. Neuropsychopharmacology 33, 320-331. doi: 10.1038/sj.npp.1301410
5. Borsini, F., Podhorna, J., and Marazziti, D. (2002). Do animal models of anxiety predict anxiolytic-like effects of antidepressants? Psychopharmacology (Berl). 163, 121-141. doi: 10.1007/s00213-002-1155-6
6. Brown, J. P., Couillard-Despres, S., Cooper-Kuhn, C. M., Winkler, J., Aigner, L., and Kuhn, H. G. (2003). Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol. 467, 1-10. doi: 10.1002/cne.10874
7. Burghardt, N. S., Park, E. H., Hen, R., and Fenton, A. A. (2012). Adult-born hippocampal neurons promote cognitive flexibility in mice. Hippocampus 22, 1795-1808. doi: 10.1002/hipo.22013
8. Caldeira, M. V., Melo, C. V., Pereira, D. B., Carvalho, R. F., Carvalho, A. L., and Duarte, C. B. (2007). BDNF regulates the expression and traffic of NMDA receptors in cultured hippocampal neurons. Mol. Cell. Neurosci. 35, 208-219. doi: 10.1016/j.mcn.2007.02.019
9. Couillard-Despres, S., Winner, B., Schaubeck, S., Aigner, R., Vroemen, M., Weidner, N., et al. (2005). Doublecortin expression levels in adult brain reflect neurogenesis. Eur. J. Neurosci. 21, 1-14. doi: 10.1111/j.1460-9568.2004.03813.x
10. Couillard-Despres, S., Wuertinger, C., Kandasamy, M., Caioni, M., Stadler, K., Aigner, R., et al. (2009). Ageing abolishes the effects of fluoxetine on neurogenesis. Mol. Psychiatry 14, 856-864. doi: 10.1038/mp.2008.147
11. Cryan, J. F., Mombereau, C., and Vassout, A. (2005). The tail suspension test as a model for assessing antidepressant activity: review of pharmacological and genetic studies in mice. Neurosci. Biobehav. Rev. 29, 571-625. doi: 10.1016/j.neubiorev.2005.03.009
12. Dalm, S., Brinks, V., van der Mark, M. H., de Kloet, E. R., and Oitzl, M. S. (2008). Non-invasive stress-free application of glucocorticoid ligands in mice. J. Neurosci. Methods 170, 77-84. doi: 10.1016/j.jneumeth.2007.12.021
13. Danielson, N. B., Kaifosh, P., Zaremba, J. D., Lovett-Barron, M., Tsai, J., Denny, C. A., et al. (2016). Distinct contribution of adult-born hippocampal granule cells to context encoding. Neuron 90, 101-112. doi: 10.1016/j.neuron.2016.02.019
14. David, D. J., Samuels, B. A., Rainer, Q., Wang, J.-W. W., Marsteller, D., Mendez, I., et al. (2009). Neurogenesis-dependent and-independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62, 479-493. doi: 10.1016/j.neuron.2009.04.017
15. Deng, W., Aimone, J. B., and Gage, F. H. (2010). New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat. Rev. Neurosci. 11, 339-350. doi: 10.1038/nrn2822
16. Denny, C. A., Burghardt, N. S., Schachter, D. M., Hen, R., and Drew, M. R. (2012). 4-to 6-week-old adult-born hippocampal neurons influence novelty-evoked exploration and contextual fear conditioning. Hippocampus 22, 1188-1201. doi: 10.1002/hipo.20964
17. Donovan, M. H., Yamaguchi, M., and Eisch, A. J. (2008). Dynamic expression of TrkB receptor protein on proliferating and maturing cells in the adult mouse dentate gyrus. Hippocampus 18, 435-439. doi: 10.1002/hipo.20410
18. Dranovsky, A., Picchini, A. M., Moadel, T., Sisti, A. C., Yamada, A., Kimura, S., et al. (2011). Experience dictates stem cell fate in the adult hippocampus. Neuron 70, 908-923. doi: 10.1016/j.neuron.2011.05.022
19. Drew, L. J., Fusi, S., and Hen, R. (2013). Adult neurogenesis in the mammalian hippocampus: why the dentate gyrus? Learn. Mem. 20, 710-729. doi: 10.1101/lm.026542.112
20. Drew, L. J., Kheirbek, M. A., Luna, V. M., Denny, C. A., Cloidt, M. A., Wu, M. V., et al. (2015). Activation of local inhibitory circuits in the dentate gyrus by adult-born neurons. Hippocampus. doi: 10.1002/hipo.22557
21. Ducottet, C., and Belzung, C. (2005). Correlations between behaviours in the elevated plus-maze and sensitivity to unpredictable subchronic mild stress: evidence from inbred strains of mice. Behav. Brain Res. 156, 153-162. doi: 10.1016/j.bbr.2004.05.018
22. Durand, M., Berton, O., Aguerre, S., Edno, L., Combourieu, I., Mormede, P., et al. (1999). Effects of repeated fluoxetine on anxiety-related behaviours, central serotonergic systems, and the corticotropic axis axis in SHR and WKY rats. Neuropharmacology 38, 893-907. doi: 10.1016/S0028-3908(99)00009-X
23. Encinas, J. M., Vaahtokari, A., and Enikolopov, G. (2006). Fluoxetine targets early progenitor cells in the adult brain. Proc. Natl. Acad. Sci. U.S.A. 103, 8233-8238. doi: 10.1073/pnas.0601992103
24. Fanselow, M. S., and Dong, H. W. (2010). Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65, 7-19. doi: 10.1016/j.neuron.2009.11.031
25. File, S. E., Ouagazzal, A. M., Gonzalez, L. E., and Overstreet, D. H. (1999). Chronic fluoxetine in tests of anxiety in rat lines selectively bred for differential 5-HT1A receptor function. Pharmacol. Biochem. Behav. 62, 695-701. doi: 10.1016/S0091-3057(98)00208-1
26. Fuss, J., Ben Abdallah, N. M., Vogt, M. A., Touma, C., Pacifici, P. G., Palme, R., et al. (2010). Voluntary exercise induces anxiety-like behavior in adult C57BL/6J mice correlating with hippocampal neurogenesis. Hippocampus 20, 364-376. doi: 10.1002/hipo.20634
27. Ge, S., Yang, C. H., Hsu, K. S., Ming, G. L., and Song, H. (2007). A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54, 559-566. doi: 10.1016/j.neuron.2007.05.002
28. Gould, E., Beylin, A., Tanapat, P., Reeves, A., and Shors, T. J. (1999). Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci. 2, 260-265. doi: 10.1038/6365
29. Griebel, G., Cohen, C., Perrault, G., and Sanger, D. J. (1999). Behavioral effects of acute and chronic fluoxetine in Wistar-Kyoto rats. Physiol. Behav. 67, 315-320. doi: 10.1016/S0031-9384(98)00298-4
30. Gross, C. G. (2000). Neurogenesis in the adult brain: death of a dogma. Nat. Rev. Neurosci. 1, 67-73. doi: 10.1038/35036235
31. Groves, J. O., Leslie, I., Huang, G. J., McHugh, S. B., Taylor, A., Mott, R., et al. (2013). Ablating adult neurogenesis in the rat has no effect on spatial processing: evidence from a novel pharmacogenetic model. PLoS Genet. 9:e1003718. doi: 10.1371/journal.pgen.1003718
32. Grubb, M. S., Nissant, A., Murray, K., and Lledo, P. M. (2008). Functional maturation of the first synapse in olfaction: development and adult neurogenesis. J. Neurosci. 28, 2919-2932. doi: 10.1523/JNEUROSCI.5550-07.2008
33. Hamilton, L. K., Joppe, S. E., Cochard, L. M., and Fernandes, K. J. (2013). Aging and neurogenesis in the adult forebrain: what we have learned and where we should go from here. Eur. J. Neurosci. 37, 1978-1986. doi: 10.1111/ejn.12207
34. Hanson, N. D., Owens, M. J., and Nemeroff, C. B. (2011). Depression, antidepressants, and neurogenesis: a critical reappraisal. Neuropsychopharmacology 36, 2589-2602. doi: 10.1038/npp.2011.220
35. Hogg, S. (1996). A review of the validity and variability of the elevated plus-maze as an animal model of anxiety. Pharmacol. Biochem. Behav. 54, 21-30. doi: 10.1016/0091-3057(95)02126-4
36. Hosmer, D. W., Lemeshow, S., and May, S. (2008). Applied Survival Analysis: Regression Modeling of Time-To-Event Data. Hoboken, NJ: Wiley-Interscience.
37. Ikrar, T., Guo, N., He, K., Besnard, A., Levinson, S., Hill, A., et al. (2013). Adult neurogenesis modifies excitability of the dentate gyrus. Front. Neural Circuits 7:204. doi: 10.3389/fncir.2013.00204
38. Imayoshi, I., Sakamoto, M., Ohtsuka, T., Takao, K., Miyakawa, T., Yamaguchi, M., et al. (2008). Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat. Neurosci. 11, 1153-1161. doi: 10.1038/nn.2185
39. Kempermann, G., Kuhn, H. G., and Gage, F. H. (1997a). Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc. Natl. Acad. Sci. U.S.A. 94, 10409-10414. doi: 10.1073/pnas.94.19.10409
40. Kempermann, G., Kuhn, H. G., and Gage, F. H. (1997b). More hippocampal neurons in adult mice living in an enriched environment. Nature 386, 493-495. doi: 10.1038/386493a0
41. Kempermann, G., Song, H., and Gage, F. H. (2015). Neurogenesis in the adult hippocampus. Cold Spring Harb. Perspect. Biol. 7:a018812. doi: 10.1101/cshperspect.a018812
42. Kheirbek, M. A., Drew, L. J., Burghardt, N. S., Costantini, D. O., Tannenholz, L., Ahmari, S. E., et al. (2013). Differential control of learning and anxiety along the dorsoventral axis of the dentate gyrus. Neuron 77, 955-968. doi: 10.1016/j.neuron.2012.12.038
43. Kheirbek, M. A., Tannenholz, L., and Hen, R. (2012). NR2B-dependent plasticity of adult-born granule cells is necessary for context discrimination. J. Neurosci. 32, 8696-8702. doi: 10.1523/JNEUROSCI.1692-12.2012
44. Klein, M., Pieri, I., Uhlmann, F., Pfizenmaier, K., and Eisel, U. (1998). Cloning and characterization of promoter and 5'-UTR of the NMDA receptor subunit epsilon 2: evidence for alternative splicing of 5'-non-coding exon. Gene 208, 259-269. doi: 10.1016/S0378-1119(98)00005-5
45. Kurt, M., Arik, A. C., and Celik, S. (2000). The effects of sertraline and fluoxetine on anxiety in the elevated plus-maze test in mice. J. Basic Clin. Physiol. Pharmacol. 11, 173-180. doi: 10.1515/JBCPP.2000.11.2.173
46. Lacefield, C. O., Itskov, V., Reardon, T., Hen, R., and Gordon, J. A. (2012). Effects of adult-generated granule cells on coordinated network activity in the dentate gyrus. Hippocampus 22, 106-116. doi: 10.1002/hipo.20860
47. Li, Y., Luikart, B. W., Birnbaum, S., Chen, J., Kwon, C. H., Kernie, S. G., et al. (2008). TrkB regulates hippocampal neurogenesis and governs sensitivity to antidepressive treatment. Neuron 59, 399-412. doi: 10.1016/j.neuron.2008.06.023
48. Li, Y., Mu, Y., and Gage, F. H. (2009). Development of neural circuits in the adult hippocampus. Curr. Top. Dev. Biol. 87, 149-174. doi: 10.1016/S0070-2153(09)01205-8
49. Lin, S. Y., Wu, K., Levine, E. S., Mount, H. T., Suen, P. C., and Black, I. B. (1998). BDNF acutely increases tyrosine phosphorylation of the NMDA receptor subunit 2B in cortical and hippocampal postsynaptic densities. Brain Res. Mol. Brain Res. 55, 20-27. doi: 10.1016/S0169-328X(97)00349-5
50. Malberg, J. E., Eisch, A. J., Nestler, E. J., and Duman, R. S. (2000). Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20, 9104-9110.
51. Monteggia, L. M., Barrot, M., Powell, C. M., Berton, O., Galanis, V., Gemelli, T., et al. (2004). Essential role of brain-derived neurotrophic factor in adult hippocampal function. Proc. Natl. Acad. Sci. U.S.A. 101, 10827-10832. doi: 10.1073/pnas.0402141101
52. Monyer, H., Burnashev, N., Laurie, D. J., Sakmann, B., and Seeburg, P. H. (1994). Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12, 529-540. doi: 10.1016/0896-6273(94)90210-0
53. Nibuya, M., Nestler, E. J., and Duman, R. S. (1996). Chronic antidepressant administration increases the expression of cAMP response element binding protein (CREB) in rat hippocampus. J. Neurosci. 16, 2365-2372.
54. Oh, J. E., Zupan, B., Gross, S., and Toth, M. (2009). Paradoxical anxiogenic response of juvenile mice to fluoxetine. Neuropsychopharmacology 34, 2197-2207. doi: 10.1038/npp.2009.47
55. Piatti, V. C., Ewell, L. A., and Leutgeb, J. K. (2013). Neurogenesis in the dentate gyrus: carrying the message or dictating the tone. Front. Neurosci. 7:50. doi: 10.3389/fnins.2013.00050
56. Revest, J. M., Dupret, D., Koehl, M., Funk-Reiter, C., Grosjean, N., Piazza, P. V., et al. (2009). Adult hippocampal neurogenesis is involved in anxiety-related behaviors. Mol. Psychiatry 14, 959-967. doi: 10.1038/mp.2009.15
57. Saarelainen, T., Hendolin, P., Lucas, G., Koponen, E., Sairanen, M., Macdonald, E., et al. (2003). Activation of the TrkB neurotrophin receptor is induced by antidepressant drugs and is required for antidepressant-induced behavioral effects. J. Neurosci. 23, 349-357.
58. Sahay, A., and Hen, R. (2007). Adult hippocampal neurogenesis in depression. Nat. Neurosci. 10, 1110-1115. doi: 10.1038/nn1969
59. Sahay, A., Scobie, K. N., Hill, A. S., O'Carroll, C. M., Kheirbek, M. A., Burghardt, N. S., et al. (2011a). Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472, 466-470. doi: 10.1038/nature09817
60. Sahay, A., Wilson, D. A., and Hen, R. (2011b). Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron 70, 582-588. doi: 10.1016/j.neuron.2011.05.012
61. Sairanen, M., Lucas, G., Ernfors, P., Castren, M., and Castren, E. (2005). Brain-derived neurotrophic factor and antidepressant drugs have different but coordinated effects on neuronal turnover, proliferation, and survival in the adult dentate gyrus. J. Neurosci. 25, 1089-1094. doi: 10.1523/JNEUROSCI.3741-04.2005
62. Samuels, B. A., Anacker, C., Hu, A., Levinstein, M. R., Pickenhagen, A., Tsetsenis, T., et al. (2015). 5-HT1A receptors on mature dentate gyrus granule cells are critical for the antidepressant response. Nat. Neurosci. 18, 1606-1616. doi: 10.1038/nn.4116
63. Samuels, B. A., Leonardo, E. D., Dranovsky, A., Williams, A., Wong, E., Nesbitt, A. M., et al. (2014). Global state measures of the dentate gyrus gene expression system predict antidepressant-sensitive behaviors. PLoS ONE 9:e85136. doi: 10.1371/journal.pone.0085136
64. Samuels, B., and Hen, R. (2011). Novelty-suppressed feeding in the mouse, in Mood and Anxiety Related Phenotypes in Mice: Characterization Using Behavioral Tests, Vol. II, ed T. D. Gould (New York, NY: Humana Press), 107-121.
65. Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., et al. (2003). Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301, 805-809. doi: 10.1126/science.1083328
66. Saxe, M. D., Battaglia, F., Wang, J.-W. W., Malleret, G., David, D. J., Monckton, J. E., et al. (2006). Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc. Natl. Acad. Sci. U.S.A. 103, 17501-17506. doi: 10.1073/pnas.0607207103
67. Scobie, K. N., Hall, B. J., Wilke, S. A., Klemenhagen, K. C., Fujii-Kuriyama, Y., Ghosh, A., et al. (2009). Krüppel-like factor 9 is necessary for late-phase neuronal maturation in the developing dentate gyrus and during adult hippocampal neurogenesis. J. Neurosci. 29, 9875-9887. doi: 10.1523/JNEUROSCI.2260-09.2009
68. Silva, R. C., and Brandao, M. L. (2000). Acute and chronic effects of gepirone and fluoxetine in rats tested in the elevated plus-maze: an ethological analysis. Pharmacol. Biochem. Behav. 65, 209-216. doi: 10.1016/S0091-3057(99)00193-8
69. Slack, S. E., Pezet, S., McMahon, S. B., Thompson, S. W., and Malcangio, M. (2004). Brain-derived neurotrophic factor induces NMDA receptor subunit one phosphorylation via ERK and PKC in the rat spinal cord. Eur. J. Neurosci. 20, 1769-1778. doi: 10.1111/j.1460-9568.2004.03656.x
70. Snyder, J. S., Kee, N., and Wojtowicz, J. M. (2001). Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J. Neurophysiol. 85, 2423-2431.
71. Snyder, J. S., Soumier, A., Brewer, M., Pickel, J., and Cameron, H. A. (2011). Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 476, 458-461. doi: 10.1038/nature10287
72. Springer, J. E., Gwag, B. J., and Sessler, F. M. (1994). Neurotrophic factor mRNA expression in dentate gyrus is increased following in vivo stimulation of the angular bundle. Brain Res. Mol. Brain Res. 23, 135-143. doi: 10.1016/0169-328X(94)90219-4
73. Srinivas, S., Watanabe, T., Lin, C. S., William, C. M., Tanabe, Y., Jessell, T. M., et al. (2001). Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1:4. doi: 10.1186/1471-213X-1-4
74. Sun, M. Y., Yetman, M. J., Lee, T. C., Chen, Y., and Jankowsky, J. L. (2014). Specificity and efficiency of reporter expression in adult neural progenitors vary substantially among nestin-CreER(T2) lines. J. Comp. Neurol. 522, 1191-1208. doi: 10.1002/cne.23497
75. Surget, A., Saxe, M., Leman, S., Ibarguen-Vargas, Y., Chalon, S., Griebel, G., et al. (2008). Drug-dependent requirement of hippocampal neurogenesis in a model of depression and of antidepressant reversal. Biol. Psychiatry 64, 293-301. doi: 10.1016/j.biopsych.2008.02.022
76. Tannenholz, L., Jimenez, J. C., and Kheirbek, M. A. (2014). Local and regional heterogeneity underlying hippocampal modulation of cognition and mood. Front. Behav. Neurosci. 8:147. doi: 10.3389/fnbeh.2014.00147
77. Venzala, E., Garcia-Garcia, A. L., Elizalde, N., Delagrange, P., and Tordera, R. M. (2012). Chronic social defeat stress model: behavioral features, antidepressant action, and interaction with biological risk factors. Psychopharmacology (Berl). 224, 313-325. doi: 10.1007/s00213-012-2754-5
78. von Engelhardt, J., Doganci, B., Jensen, V., Hvalby, Ò., Göngrich, C., Taylor, A., et al. (2008). Contribution of hippocampal and extra-hippocampal NR2B-containing NMDA receptors to performance on spatial learning tasks. Neuron 60, 846-860. doi: 10.1016/j.neuron.2008.09.039
79. Wang, J.-W. W., David, D. J., Monckton, J. E., Battaglia, F., and Hen, R. (2008). Chronic fluoxetine stimulates maturation and synaptic plasticity of adult-born hippocampal granule cells. J. Neurosci. 28, 1374-1384. doi: 10.1523/JNEUROSCI.3632-07.2008
80. Wu, M. V., and Hen, R. (2014). Functional dissociation of adult-born neurons along the dorsoventral axis of the dentate gyrus. Hippocampus 24, 751-761. doi: 10.1002/hipo.22265
81. Zafra, F., Castren, E., Thoenen, H., and Lindholm, D. (1991). Interplay between glutamate and gamma-aminobutyric acid transmitter systems in the physiological regulation of brain-derived neurotrophic factor and nerve growth factor synthesis in hippocampal neurons. Proc. Natl. Acad. Sci. U.S.A. 88, 10037-10041. doi: 10.1073/pnas.88.22.10037
82. Zhao, C., Deng, W., and Gage, F. H. (2008). Mechanisms and functional implications of adult neurogenesis. Cell 132, 645-660. doi: 10.1016/j.cell.2008.01.033