Sigma-1 receptor knockout impairs neurogenesis in dentate gyrus of adult hippocampus via down-regulation of nmda receptors

CNS Neuroscience and Therapeutics

Volumn 19, Issue 9, 2013, Pages 705-713

  Sha, Sha ^a   Qu, Wei Jun ^a   Li, Lin ^a   Lu, Zi Hong ^a   Chen, Lei ^a   Yu, Wen Feng ^b   Chen, Ling ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

^b GUIZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Aminobutyric acid; Hippocampus; N methyl d aspartate receptor; Neurogenesis; Sigma 1 receptor

Indexed keywords

BROXURIDINE; GLIAL FIBRILLARY ACIDIC PROTEIN; KI 67 ANTIGEN; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; NEURON SPECIFIC NUCLEAR PROTEIN; SIGMA 1 OPIATE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DENSITY; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; DOWN REGULATION; GENE SILENCING; GRANULAR CELL; HIPPOCAMPUS; MALE; MITOSIS; MOUSE; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; PATCH CLAMP; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STEM CELL;

HIPPOCAMPUS; N-METHYL-D-ASPARTATE RECEPTOR; NEUROGENESIS; SIGMA-1 RECEPTOR; Γ-AMINOBUTYRIC ACID;

ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; CELL PROLIFERATION; DENTATE GYRUS; DOWN-REGULATION; MALE; MICE; N-METHYLASPARTATE; NEURITES; NEUROGENESIS; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, SIGMA;

EID: 84882817586     PISSN: 17555930     EISSN: 17555949     Source Type: Journal    
DOI: 10.1111/cns.12129     Document Type: Article

References (56)

1. 25-35-amyloid peptide-induced amnesia in mice through a common mechanism. Neuroscience 1998;83:413-428.
2. Maurice T. Beneficial effect of the sigma(1) receptor agonist PRE-084 against the spatial learning deficits in aged rats. Eur J Pharmacol 2001;431:223-227.
3. Frye CA. The role of neurosteroids and nongenomic effects of progestins in the ventral tegmental area in mediating sexual receptivity of rodents. Horm Behav 2001;40:226-233.
4. Vallee M, Mayo W, Koob GF, Le Moal M. Neurosteroids in learning and memory processes. Int Rev Neurobiol 2001;46:273-320.
5. Schumacher M, Weill-Engerer S, Liere P, et al. Steroid hormones and neurosteroids in normal and pathological aging of the nervous system. Prog Neurobiol 2003;71:3-29.
6. Barbaccia ML. Neurosteroidogenesis: Relevance to neurosteroid actions in brain and modulation by psychotropic drugs. Crit Rev Neurobiol 2004;16:67-74.
7. Maurice T. Neurosteroids and sigma1 receptors, biochemical and behavioral relevance. Pharmacopsychiatry 2004;37:S171-S182.
8. Monnet FP, Maurice T. The sigma1 protein as a target for the non-genomic effects of neuro(active)steroids: Molecular, physiological, and behavioral aspects. J Pharmacol Sci 2006;100:93-118.
9. Christie BR, Cameron HA. Neurogenesis in the adult hippocampus. Hippocampus 2006;16:199-207.
10. Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza PV, Abrous DN. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc Natl Acad Sci USA 2003;100:14385-14390.
11. Bruel-Jungerman E, Laroche S, Rampon C. New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur J Neurosci 2005;21:513-521.
12. Hayashi T, Su TP. Sigma-1 receptors at galactosylceramide-enriched lipid microdomains regulate oligodendrocyte differentiation. Proc Natl Acad Sci USA 2004;101:14949-14954.
13. Takebayashi M, Hayashi T, Su TP. Nerve growth factor-induced neurite sprouting in PC12 cells involves sigma-1 receptors: Implications for antidepressants. J Pharmacol Exp Ther 2002;303:1227-1237.
14. Yang R, Zhou R, Chen L, Cai W, Tomimoto H, Sokabe M. Pregnenolone sulfate enhances survival of adult-generated hippocampal granule cells via sustained presynaptic potentiation. Neuropharmacology 2011;60:529-541.
15. Azizi H, Mehrjardi NZ, Shahbazi E, Hemmesi K, Bahmani MK, Baharvand H. Dehydroepiandrosterone stimulates neurogenesis in mouse embryonal carcinoma cell- and human embryonic stem cell-derived neural progenitors and induces dopaminergic neurons. Stem Cells Dev 2010;19:809-818.
16. 25-35-impaired survival of newborn neurons in the dentate gyrus through a modulation of PI3K-Akt-mTOR signaling. Neuropharmacology 2010;59:323-333.
17. Karishma KK, Herbert J. Dehydroepiandrosterone (DHEA) stimulates neurogenesis in the hippocampus of the rat, promotes survival of newly formed neurons and prevents corticosterone-induced suppression. Eur J Neurosci 2002;16:445-453.
18. Monnet FP, Debonnel G, Junien JL, De Montigny C. N-methyl-d-aspartate-induced neuronal activation is selectively modulated by sigma receptors. Eur J Pharmacol 1990;179:441-445.
19. Chen L, Miyamoto Y, Furuya K, Mori N, Sokabe M. PREGS induces LTP in the hippocampal dentate gyrus of adult rats via the tyrosine phosphorylation of NR2B coupled to ERK/CREB [corrected] signaling. J Neurophysiol 2007;98:1538-1548.
20. Martina M, Turcotte ME, Halman S, Bergeron R. The sigma-1 receptor modulates NMDA receptor synaptic transmission and plasticity via SK channels in rat hippocampus. J Physiol 2007;578:143-157.
21. Nuwayhid SJ, Werling LL. Sigma1 receptor agonist-mediated regulation of N-methyl-d-aspartate-stimulated [3H]dopamine release is dependent upon protein kinase C. J Pharmacol Exp Ther 2003;304:364-369.
22. Mtchedlishvili Z, Kapur J. A presynaptic action of the neurosteroid pregnenolone sulfate on GABAergic synaptic transmission. Mol Pharmacol 2003;64:857-864.
23. Sabino V, Cottone P, Parylak SL, Steardo L, Zorrilla EP. Sigma-1 receptor knockout mice display a depressive-like phenotype. Behav Brain Res 2009;198:472-476.
24. Chevallier N, Keller E, Maurice T. Behavioural phenotyping of knockout mice for the sigma-1 (sigma(1)) chaperone protein revealed gender-related anxiety, depressive-like and memory alterations. J Psychopharmacol 2011;25:960-975.
25. Pietranera L, Lima A, Roig P, De Nicola AF. Involvement of brain-derived neurotrophic factor and neurogenesis in oestradiol neuroprotection of the hippocampus of hypertensive rats. J Neuroendocrinol 2010;22:1082-1092.
26. Chiou CS, Huang CC, Liang YC, Tsai YC, Hsu KS. Impairment of long-term depression in the anterior cingulate cortex of mice with bone cancer pain. Pain 2012;153:2097-2108.
27. Cameron HA, McEwen BS, Gould E. Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J Neurosci 1995;15:4687-4692.
28. 25-35-injected mice through sigma1 receptor- and alpha7nAChR-mediated neuroprotection. Neuropharmacology 2012;63:1042-1050.
29. Hayes NL, Nowakowski RS. Dynamics of cell proliferation in the adult dentate gyrus of two inbred strains of mice. Brain Res Dev Brain Res 2002;134:77-85.
30. Scholzen T, Gerdes J. The Ki-67 protein: From the known and the unknown. J Cell Physiol 2000;182:311-322.
31. Kempermann G, Jessberger S, Steiner B, Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 2004;27:447-452.
32. Rao MS, Shetty AK. Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur J Neurosci 2004;19:234-246.
33. Monnet FP, Mahe V, Robel P, Baulieu EE. Neurosteroids, via sigma receptors, modulate the [3H]norepinephrine release evoked by N-methyl-d-aspartate in the rat hippocampus. Proc Natl Acad Sci USA 1995;92:3774-3778.
34. Kim HW, Kwon YB, Roh DH, et al. Intrathecal treatment with sigma1 receptor antagonists reduces formalin-induced phosphorylation of NMDA receptor subunit 1 and the second phase of formalin test in mice. Br J Pharmacol 2006;148:490-498.
35. Nacher J, McEwen BS. The role of N-methyl-d-asparate receptors in neurogenesis. Hippocampus 2006;16:267-270.
36. Deisseroth K, Singla S, Toda H, Monje M, Palmer TD, Malenka RC. Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 2004;42:535-552.
37. Nacher J, Alonso-Llosa G, Rosell DR, McEwen BS. NMDA receptor antagonist treatment increases the production of new neurons in the aged rat hippocampus. Neurobiol Aging 2003;24:273-284.
38. Pincus DW, DiCicco-Bloom E, Black IB. Role of voltage-sensitive calcium channels in mitogenic stimulation of neuroblasts. Brain Res 1991;553:211-214.
39. Kitayama T, Yoneyama M, Tamaki K, Yoneda Y. Possible regulation by N-methyl-d-aspartate receptors of proliferative progenitor cells expressed in adult mouse hippocampal dentate gyrus. J Neurochem 2003;84:767-780.
40. Hetman M, Kharebava G. Survival signaling pathways activated by NMDA receptors. Curr Top Med Chem 2006;6:787-799.
41. Hardingham GE, Fukunaga Y, Bading H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 2002;5:405-414.
42. Tashiro A, Zhao C, Gage FH. Retrovirus-mediated single-cell gene knockout technique in adult newborn neurons in vivo. Nat Protoc 2006;1:3049-3055.
43. Zhao C, Teng EM, Summers RG Jr, Ming GL, Gage FH. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 2006;26:3-11.
44. Compagnone NA, Mellon SH. Dehydroepiandrosterone: A potential signalling molecule for neocortical organization during development. Proc Natl Acad Sci USA 1998;95:4678-4683.
45. Alonso G, Phan V, Guillemain I, et al. Immunocytochemical localization of the sigma(1) receptor in the adult rat central nervous system. Neuroscience 2000;97:155-170.
46. Brinton RD. The neurosteroid 3 alpha-hydroxy-5 alpha-pregnan-20-one induces cytoarchitectural regression in cultured fetal hippocampal neurons. J Neurosci 1994;14:2763-2774.
47. MacLusky NJ, Hajszan T, Leranth C. Effects of dehydroepiandrosterone and flutamide on hippocampal CA1 spine synapse density in male and female rats: Implications for the role of androgens in maintenance of hippocampal structure. Endocrinology 2004;145:4154-4161.
48. Hajszan T, MacLusky NJ, Leranth C. Dehydroepiandrosterone increases hippocampal spine synapse density in ovariectomized female rats. Endocrinology 2004;145:1042-1045.
49. Zhang L, Li BS, Ma W, et al. Dehydroepiandrosterone (DHEA) and its sulfated derivative (DHEAS) regulate apoptosis during neurogenesis by triggering the Akt signaling pathway in opposing ways. Brain Res Mol Brain Res 2002;98:58-66.
50. Yagasaki Y, Numakawa T, Kumamaru E, Hayashi T, Su TP, Kunugi H. Chronic antidepressants potentiate via sigma-1 receptors the brain-derived neurotrophic factor-induced signaling for glutamate release. J Biol Chem 2006;281:12941-12949.
51. Xu B, Yang R, Chang F, Chen L, Xie G, Sokabe M. Neurosteroid PREGS protects neurite growth and survival of newborn neurons in the hippocampal dentate gyrus of APPswe/PS1dE9 mice. Curr Alzheimer Res 2012;9:361-372.
52. Leuner B, Gould E, Shors TJ. Is there a link between adult neurogenesis and learning? Hippocampus 2006;16:216-224.
53. Thuret S, Toni N, Aigner S, Yeo GW, Gage FH. Hippocampus-dependent learning is associated with adult neurogenesis in MRL/MpJ mice. Hippocampus 2009;19:658-669.
54. Schaffer DV, Gage FH. Neurogenesis and neuroadaptation. Neuromolecular Med 2004;5:1-9.
55. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. Functional neurogenesis in the adult hippocampus. Nature 2002;415:1030-1034.
56. Chun SK, Sun W, Park JJ, Jung MW. Enhanced proliferation of progenitor cells following long-term potentiation induction in the rat dentate gyrus. Neurobiol Learn Mem 2006;86:322-329.