Stressor-specific regulation of distinct brain-derived neurotrophic factor transcripts and cyclic AMP response element-binding protein expression in the postnatal and adult rat hippocampus

Neuropsychopharmacology

Volumn 32, Issue 7, 2007, Pages 1504-1519

  Nair, Amrita ^a   Vadodaria, Krishna C ^a   Banerjee, Sunayana B ^a   Benekareddy, Madhurima ^a   Dias, Brian G ^a   Duman, Ronald S ^b   Vaidya, Vidita A ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

BDNF exon; Dentate gyrus; Immobilization stress; Maternal separation; Neurogenesis; Progenitor

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MESSENGER RNA;

ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL PROLIFERATION; CHRONIC STRESS; CONTROLLED STUDY; DEPRESSION; DISEASE PREDISPOSITION; EARLY LIFE STRESS; EXON; GENE EXPRESSION REGULATION; HIPPOCAMPUS; IMMOBILIZATION STRESS; MALE; MATERNAL DEPRIVATION; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN VARIANT; REGULATORY MECHANISM; STEM CELL; TIME; TRANSCRIPTION REGULATION; UPREGULATION;

AGING; ANIMALS; ANIMALS, NEWBORN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DIFFERENTIATION; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; MALE; MATERNAL DEPRIVATION; NEURAL PATHWAYS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; STEM CELLS; STRESS, PSYCHOLOGICAL; TRANS-ACTIVATION (GENETICS); UP-REGULATION;

EID: 34250356437     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1301276     Document Type: Article

References (65)

1. Alfonso J, Frick LR, Silberman DM, Palumbo ML, Genaro AM, Frasch AC (2006). Regulation of hippocampal gene expression is conserved in two species subjected to different stressors and antidepressant treatments. Biol Psychiatry 59: 244-251.
2. Barco A, Patterson S, Alarcon JM, Gromova P, Mata-Roig M, Morozov A et al (2005). Gene expression profiling of facilitated L-LTP in VP16-CREB mice reveals that BDNF is critical for the maintenance of LTP and its synaptic capture. Neuron 48: 123-137.
3. Bender RA, Lauterborn JC, Gall CM, Cariaga W, Baram TZ (2001). Enhanced CREB phosphorylation in immature dentate gyrus granule cells precedes neurotrophin expression and indicates a specific role of CREB in granule cell differentiation. Eur J Neurosci 13: 679-686.
4. Blendy JA (2006). The role of CREB in depression and antidepressant treatment. Biol Psychiatry 59: 1144-1150.
5. Branchi I, Francia N, Alleva E (2004). Epigenetic control of neurobehavioural plasticity: the role of neurotrophins. Behav Pharmacol 15: 353-362.
6. Bremner JD, Narayan M, Anderson ER, Staib LH, Miller HL, Charney DS (2000). Hippocampal volume reduction in major depression. Am J Psychiatry 157: 115-118.
7. Brunson KL, Chen Y, Avishai-Eliner S, Baram TZ (2003). Stress and the developing hippocampus: a double-edged sword? Mol Neurobiol 27: 121-136.
8. Buwalda B, Kole MH, Veenema AH, Huininga M, de Boer SF, Korte SM et al (2005). Long-term effects of social stress on brain and behavior: a focus on hippocampal functioning. Neurosci Biobehav Rev 29: 83-97.
9. Conti AC, Cryan JF, Dalvi A, Lucki I, Blendy JA (2002). cAMP response element-binding protein is essential for the upregulation of brain-derived neurotrophic factor transcription, but not the behavioral or endocrine responses to antidepressant drugs. J Neurosci 22: 3262-3268.
10. Dennis KE, Levitt P (2005). Regional expression of brain derived neurotrophic factor (BDNF) is correlated with dynamic patterns of promoter methylation in the developing mouse forebrain. Mol Brain Res 140: 1-9.
11. Dias BG, Banerjee SB, Duman RS, Vaidya VA (2003). Differential regulation of brain derived neurotrophic factor transcripts by antidepressant treatments in the adult rat brain. Neuropharmacology 45: 553-563.
12. Duman RS (2004). Role of neurotrophic factors in the etiology and treatment of mood disorders. Neuromolecular Med 5: 11-25.
13. Fujioka T, Fujioka A, Duman RS (2004). Activation of cAMP signaling facilitates the morphological maturation of newborn neurons in adult hippocampus. J Neurosci 24: 319-328.
14. Garoflos E, Stamatakis A, Mantelas A, Philippidis H, Stylianopoulou F (2005). Cellular mechanisms underlying an effect of 'early handling' on pCREB and BDNF in the neonatal rat hippocampus. Brain Res 1052: 187-195.
15. Gomez-Pinilla F, Vaynman S (2005). A 'deficient environment' in prenatal life may compromise systems important for cognitive function by affecting BDNF in the hippocampus. Exp Neurol 192: 235-243.
16. Gould E, Woolley CS, McEwen BS (1991). Adrenal steroids regulate postnatal development of the rat dentate gyrus: I. Effects of glucocorticoids on cell death. J Comp Neurol 313: 479-485.
17. Greisen MH, Altar CA, Bolwig TG, Whitehead R, Wortwein G (2005). Increased adult hippocampal brain-derived neurotrophic factor and normal levels of neurogenesis in maternal separation rats. J Neurosci Res 79: 772-778.
18. Heim C, Nemeroff CB (2002). Neurobiology of early life stress: clinical studies. Semin Clin Neuropsychiatry 7: 147-159.
19. Josselyn SA, Nguyen PV (2005). CREB, synapses and memory disorders: past progress and future challenges. Curr Drug Targets CNS Neurol Disord 4: 481-497.
20. Kalinichev M, Easterling KW, Plotsky PM, Holtzman SG (2002). Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long-Evans rats. Pharmacol Biochem Behav 73: 131-140.
21. Ladd CO, Huot RL, Thrivikraman KV, Nemeroff CB, Meaney MJ, Plotsky PM (2000). Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog Brain Res 122: 81-103.
22. Lai IC, Hong CJ, Tsai SJ (2003). Expression of cAMP response element-binding protein in major depression before and after antidepressant treatment. Neuropsychobiology 48: 182-185.
23. Lauterborn JC, Rivera S, Stinis CT, Hayes VY, Isackson PJ, Gall CM (1996). Differential effects of protein synthesis inhibition on the activity-dependent expression of BDNF transcripts: evidence for immediate-early gene responses from specific promoters. J Neurosci 16: 7428-7436.
24. Liu D, Diorio J, Day JC, Francis DD, Meaney MJ (2000). Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci 3: 799-806.
25. Lu B, Gottschalk W (2000). Modulation of hippocampal synaptic transmission and plasticity by neurotrophins. Prog Brain Res 128: 231-241.
26. Magarinos AM, McEwen BS, Flugge G, Fuchs E (1996). Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci 16: 3534-3540.
27. Marmigere F, Givalois L, Rage F, Arancibia S, Tapia-Arancibia L (2003). Rapid induction of BDNF expression in the hippocampus during immobilization stress challenge in adult rats. Hippocampus 13: 646-655.
28. McEwen BS (2004). Protection and damage from acute and chronic stress: allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Ann NY Acad Sci 1032: 1-7.
29. Meaney MJ, Szyf M (2005). Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome. Dialogues Clin Neurosci 7: 103-123.
30. Mirescu C, Gould E (2006). Stress and adult neurogenesis. Hippocampus 16: 233-238.
31. Mirescu C, Peters JD, Gould E (2004). Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 7: 841-846.
32. Nakagawa S, Kim JE, Lee R, Malberg JE, Chen J, Steffen C et al (2002). Regulation of neurogenesis in adult mouse hippocampus by cAMP and the cAMP response element-binding protein. J Neurosci 22: 3673-3682.
33. Nibuya M, Nestler EJ, Duman RS (1996). Chronic antidepressant administration increases the expression of cAMP response element binding protein (CREB) in rat hippocampus. J Neurosci 16: 2365-2372.
34. Nibuya M, Takahashi M, Russell DS, Duman RS (1999). Repeated stress increases catalytic TrkB mRNA in rat hippocampus. Neurosci Lett 267: 81-84.
35. Ortiz J, Fitzgerald LW, Lane S, Terwilliger R, Nestler EJ (1996). Biochemical adaptations in the mesolimbic dopamine system in response to repeated stress. Neuropsychopharmacology 14: 443-452.
36. Pacak K, Palkovits M (2001). Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr Rev 22: 502-548.
37. Park HJ, Lim S, Lee HS, Lee HJ, Yoo YM, Lee HJ et al (2002). Acupuncture enhances cell proliferation in dentate gyrus of maternally-separated rats. Neurosci Lett 319: 153-156.
38. Pencea V, Bingaman KD, Wiegand SJ, Luskin MB (2001). Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J Neurosci 21: 6706-6717.
39. Pham K, Nacher J, Hof PR, McEwen BS (2003). Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur J Neurosci 17: 879-886.
40. Pryce CR, Bettschen D, Feldon J (2001). Comparison of the effects of early handling and early deprivation on maternal care in the rat. Dev Psychobiol 38: 239-251.
41. Radley JJ, Morrison JH (2005). Repeated stress and structural plasticity in the brain. Ageing Res Rev 4: 271-287.
42. Roceri M, Cirulli F, Pessina C, Peretto P, Racagni G, Riva MA (2004). Postnatal repeated maternal deprivation produces age-dependent changes of brain-derived neurotrophic factor expression in selected rat brain regions. Biol Psych 55: 708-714.
43. Roceri M, Hendriks W, Racagni G, Ellenbroek BA, Riva MA (2002). Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus. Mol Psychiatry 7: 609-616.
44. Russo-Neustadt AA, Beard RC, Huang YM, Cotman CW (2000). Physical activity and antidepressant treatment potentiate the expression of specific brain-derived neurotrophic factor transcripts in the rat hippocampus. Neuroscience 101: 305-312.
45. Sairanen M, Lucas G, Ernfors P, Castren M, 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.
46. 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.
47. Sathanoori M, Dias BG, Nair AR, Banerjee SB, Tole S, Vaidya VA (2004). Differential regulation of multiple brain-derived neurotrophic factor transcripts in the postnatal and adult rat hippocampus during development, and in response to kainate administration. Mol Brain Res 130: 170-177.
48. Schlessinger AR, Cowan WM, Gottlieb DI (1975). An autoradio-graphic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J Comp Neurol 159: 149-175.
49. Shieh PB, Hu SC, Bobb K, Timmusk T, Ghosh A (1998). Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron 20: 727-740.
50. Silva R, Lu J, Wu Y, Martins L, Almeida O, Sousa N (2006). Mapping cellular gains and losses in the postnatal dentate gyrus: implications for psychiatric disorders. Exp Neurol 200: 321-323.
51. Smith MA, Makino S, Kvetnansky R, Post RM (1995). Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J Neurosci 15: 1768-1777.
52. Smith ME (2005). Bilateral hippocampal volume reduction in adults with post-traumatic stress disorder: a meta-analysis of structural MRI studies. Hippocampus 15: 798-807.
53. Song L, Che W, Min-Wei W, Murakami Y, Matsumoto K (2006). Impairment of the spatial learning and memory induced by learned helplessness and chronic mild stress. Pharmacol Biochem Behav 83: 186-193.
54. Tabuchi A, Sakaya H, Kisukeda T, Fushiki H, Tsuda M (2002). Involvement of an upstream stimulatory factor as well as cAMP-responsive element-binding protein in the activation of brain-derived neurotrophic factor gene promoter I. J Biol Chem 277: 35920-35931.
55. Timmusk T, Belluardo N, Persson H, Metsis M (1994). Developmental regulation of brain-derived neurotrophic factor messenger RNAs transcribed from different promoters in the rat brain. Neuroscience 60: 287-291.
56. Timmusk T, Lendahl U, Funakoshi H, Arenas E, Persson H, Metsis M (1995). Identification of brain-derived neurotrophic factor promoter regions mediating tissue-specific, axotomy-, and neuronal activity-induced expression in transgenic mice. J Cell Biol 128: 185-199.
57. Timmusk T, Palm K, Metsis M, Reintam T, Paalme V, Saarma M et al (1993). Multiple promoters direct the tissue specific expression of the rat BDNF gene. Neuron 10: 475-489.
58. Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ (2006). Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci 9: 519-525.
59. Vallee M, Mayo W, Dellu F, Le Moal M, Simon H, Maccari S (1997). Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J Neurosci 17: 2626-2636.
60. Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S (2002). Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22: 6810-6818.
61. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR et al (2004). Epigenetic programming by maternal behavior. Nat Neurosci 7: 847-854.
62. Xing J, Ginty DD, Greenberg ME (1996). Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273: 959-963.
63. Yamada S, Yamamoto M, Ozawa H, Riederer P, Saito T (2003). Reduced phosphorylation of cyclic AMP-responsive element binding protein in the postmortem orbitofrontal cortex of patients with major depressive disorder. J Neural Transm 110: 671-680.
64. Zhang LX, Levine S, Dent G, Zhan Y, Xing G, Okimoto D et al (2002). Maternal deprivation increases cell death in the infant rat brain. Brain Res Dev Brain Res 133: 1-11.
65. Zhao C, Teng EM, Summers Jr RG, Ming GL, Gage FH (2006). Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26: 3-11.