Cellular mechanisms underlying the effect of a single exposure to neonatal handling on neurotrophin-3 in the brain of 1-day-old rats

Neuroscience

Volumn 148, Issue 2, 2007, Pages 349-358

  Garoflos, E ^a   Stamatakis, A ^a   Pondiki, S ^a   Apostolou, A ^a   Philippidis, H ^a   Stylianopoulou, F ^a  

^a UNIVERSITY OF ATHENS   (Greece)

Author keywords

cortex; early handling; hippocampus; L type voltage gated Ca2+ channels; neurotransmitter receptors; neurotrophin 3

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMPA RECEPTOR ANTAGONIST; CALCIUM CHANNEL L TYPE; KAINIC ACID; KAINIC ACID RECEPTOR ANTAGONIST; MORPHOGEN; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NEUROTROPHIN 3;

ACUTE STRESS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CALCIUM CELL LEVEL; CELL ACTIVITY; CONTROLLED STUDY; COPING BEHAVIOR; FEMALE; HIPPOCAMPUS; MALE; MATERNAL BEHAVIOR; MATERNAL CARE; NEUROTRANSMISSION; NEWBORN; NEWBORN CARE; NONHUMAN; PARIETAL LOBE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BRAIN; EXCITATORY AMINO ACID ANTAGONISTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HANDLING (PSYCHOLOGY); MATERNAL BEHAVIOR; NEURONS; NEUROTROPHIN 3; RATS; RATS, WISTAR; TIME FACTORS;

EID: 34548439009     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.06.020     Document Type: Article

References (62)

1. Baker R.E., Dijkhuizen P.A., Van Pelt J., and Verhaagen J. Growth of pyramidal, but not non-pyramidal, dendrites in long-term organotypic explants of neonatal rat neocortex chronically exposed to neurotrophin-3. Eur J Neurosci 10 (1998) 1037-1044
2. Ben-Ari Y. Developing networks play a similar melody. Trends Neurosci 24 (2001) 353-360
3. Ben-Ari Y. Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3 (2002) 728-739
4. Bilsland J.G., and Harper S.J. Quantification of Fos immunoreactivity in cortical cultures treated with growth factors. J Neurosci Methods 84 (1998) 121-130
5. Boukhaddaoui H., Sieso V., Scamps F., and Valmier J. An activity-dependent neurotrophin-3 autocrine loop regulates the phenotype of developing hippocampal pyramidal neurons before target contact. J Neurosci 21 (2001) 8789-8797
6. Caldji C., Francis D., Sharma S., Plotsky P.M., and Meaney M.J. The effects of early rearing environment on the development of GABAA and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacology 22 (2000) 219-229
7. Champagne F.A., Francis D.D., Mar A., and Meaney M.J. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 79 (2003) 359-371
8. Collazo D., Takahashi H., and McKay R.D. Cellular targets and trophic functions of neurotrophin-3 in the developing rat hippocampus. Neuron 9 (1992) 643-656
9. Das K.P., Chao S.L., White L.D., Haines W.T., Harry G.J., Tilson H.A., and Barone Jr. S. Differential patterns of nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3 mRNA and protein levels in developing regions of rat brain. Neuroscience 103 (2001) 739-761
10. Engele J., and Schilling K. Growth factor-induced c-fos expression defines distinct subsets of midbrain dopaminergic neurons. Neuroscience 73 (1996) 397-406
11. Escorihuela R.M., Tobena A., and Fernandez-Teruel A. Environmental enrichment reverses the detrimental action of early inconsistent stimulation and increases the beneficial effects of postnatal "handling" on shuttlebox learning in adult rats. Behav Brain Res 2 (1994) 169-173
12. Fenoglio K.A., Brunson K.L., Avishai-Eliner S., Stone B.A., Kapadia B.J., and Baram T.Z. Enduring, handling-evoked enhancement of hippocampal memory function and glucocorticoid receptor expression involves activation of the corticotrophin-releasing factor type 1 receptor. Endocrinology 146 (2005) 4090-4096
13. Fenoglio K.A., Chen Y., and Baram T.Z. Neuroplasticity of the hypothalamic-pituitary-adrenal axis early in life requires recurrent recruitment of stress-regulating brain regions. J Neurosci 26 (2006) 2434-2442
14. Fernandez-Teruel A., Escorihuela R.M., Castellano B., Gonzalez B., and Tobena A. Neonatal handling and environmental enrichment effects on emotionality, novelty/reward seeking, and age-related cognitive and hippocampal impairments: focus on the Roman rat lines. Behav Genet 27 (1997) 513-526
15. Fernandez-Teruel A., Gimenez-Llort L., Escorihuela R.M., Gil L., Aguilar R., Steimer T., and Tobena A. Early-life handling stimulation and environmental enrichment. Are some of their effects mediated by similar neural mechanisms?. Pharmacol Biochem Behav 73 (2002) 233-245
16. Friedman W.J., Ernfors P., and Persson H. Transient and persistent expression of NT-3/HDNF mRNA in the rat brain during postnatal development. J Neurosci 11 (1991) 1577-1584
17. Garoflos E., Panagiotaropoulos T., Pondiki S., Stamatakis A., Philippidis E., and Stylianopoulou F. Cellular mechanisms underlying the effects of an early experience on cognitive abilities and affective states. Ann Gen Psychiatry 4 (2005) 8-19
18. Garoflos E., Stamatakis A., Mantelas A., Philippidis H., and Stylianopoulou F. Cellular mechanisms underlying an effect of "early handling" on pCREB and BDNF in the neonatal rat hippocampus. Brain Res 1052 (2005) 187-195
19. Giordano T., Pan J.B., Casuto D., Watanabe S., and Arneric S.P. Thyroid hormone regulation of NGF, NT-3 and BDNF RNA in the adult rat brain. Brain Res Mol Brain Res 16 (1992) 239-245
20. Huang E.J., and Reichardt L.F. Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72 (2003) 609-642
21. Huot R.L., Plotsky P.M., Lenox R.H., and McNamara R.K. Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Res 950 (2002) 52-63
22. Ickes B.R., Pham T.M., Sanders L.A., Albeck D.S., Mohammed A.H., and Granholm A.C. Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain. Exp Neurol 164 (2000) 45-52
23. Ip N.Y., Li Y., Yancopoulos G.D., and Lindsay R.M. Cultured hippocampal neurons show responses to BDNF, NT-3, and NT-4, but not NGF. J Neurosci 13 (1993) 3394-3405
24. Ishibashi H., Hihara S., Takahashi M., Heike T., Yokota T., and Iriki A. Tool-use learning selectively induces expression of brain-derived neurotrophic factor, its receptor trkB, and neurotrophin 3 in the intraparietal multisensory cortex of monkeys. Brain Res Cogn Brain Res 14 (2002) 3-9
25. Ishimaru N., Tabuchi A., Hara D., Hayashi H., Sugimoto T., Yasuhara M., Shiota J., and Tsuda M. Regulation of neurotrophin-3 gene transcription by Sp3 and Sp4 in neurons. J Neurochem 100 (2007) 520-531
26. Johnson J.R., Chu A.K., and Sato-Bigbee C. Possible role of CREB in the stimulation of oligodendrocyte precursor cell proliferation by neurotrophin-3. J Neurochem 74 (2000) 1409-1417
27. Jutapakdeegul N., Casalotti S.O., Govitrapong P., and Kotchabhakdi N. Postnatal touch stimulation acutely alters corticosterone levels and glucocorticoid receptor gene expression in the neonatal rat. Dev Neurosci 25 (2003) 26-33
28. Kim H.S., Lee S.J., Kim D.S., and Cho H.J. Effects of brain-derived neurotrophic factor and neurotrophin-3 on expression of mRNAs encoding c-Fos, neuropeptides and glutamic acid decarboxylase in cultured spinal neurons. Neuroreport 11 (2000) 3873-3876
29. Levine S. Maternal behavior as a mediator of pup adrenocortical function. Ann N Y Acad Sci 746 (1994) 260-275
30. Lindholm D., Castren E., Tsoulfas P., Kolbeck R., Berzaghi Mda P., Leingartner A., Heisenberg C.P., Tessarollo L., Parada L.F., and Thoenen H. Neurotrophin-3 induced by tri-iodothyronine in cerebellar granule cells promotes Purkinje cell differentiation. J Cell Biol 122 (1993) 443-450
31. Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A., Sharma S., Pearson D., Plotsky P.M., and Meaney M.J. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277 (1997) 1620-1621
32. Lu B., Pang P.T., and Woo N.H. The yin and yang of neurotrophin action. Nat Rev Neurosci 6 (2005) 603-614
33. Luesse H.G., Roskoden T., Linke R., Otten U., Heese K., and Schwegler H. Modulation of mRNA expression of the neurotrophins of the nerve growth factor family and their receptors in the septum and hippocampus of rats after transient postnatal thyroxine treatment. I. Expression of nerve growth factor, brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin 4 mRNA. Exp Brain Res 119 (1998) 1-8
34. Maisonpierre P.C., Belluscio L., Friedman B., Alderson R.F., Wiegand S.J., Furth M.E., Lindsay R.M., and Yancopoulos G.D. NT-3, BDNF, and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression. Neuron 5 (1990) 501-509
35. Mao X., Yang S.H., Simpkins J.W., and Barger S.W. Glutamate receptor activation evokes calpain-mediated degradation of Sp3 and Sp4, the prominent Sp-family transcription factors in neurons. J Neurochem 100 (2007) 1300-1314
36. McAllister A.K., Katz L.C., and Lo D.C. Neurotrophins and synaptic plasticity. Annu Rev Neurosci 22 (1999) 295-318
37. McCormick C.M., Kehoe P., and Kovacs S. Corticosterone release in response to repeated, short episodes of neonatal isolation: evidence of sensitization. Int J Dev Neurosci 16 (1998) 175-185
38. Meaney M.J., and Aitken D.H. The effects of early postnatal handling on hippocampal glucocorticoid receptor concentrations: temporal parameters. Brain Res 354 (1985) 301-304
39. Meaney M.J., Aitken D.H., and Sapolsky R.M. Thyroid hormones influence the development of hippocampal glucocorticoid receptors in the rat: a mechanism for the effects of postnatal handling on the development of the adrenocortical stress response. Neuroendocrinology 45 (1987) 278-283
40. Meaney M.J., Aitken D.H., Van Berkel C., Bhatnagar S., and Sapolsky R.M. Effect of neonatal handling on age-related impairments associated with the hippocampus. Science 239 (1988) 766-768
41. Meaney M.J., Diorio J., Francis D., Weaver S., Yau J., Chapman K., and Seckl J.R. Postnatal handling increases the expression of cAMP-inducible transcription factors in the rat hippocampus: the effects of thyroid hormones and serotonin. J Neurosci 20 (2000) 3926-3935
42. Meaney M.J., Mitchell J.B., Aitken D.H., Bhatnagar S., Bodnoff S.R., Iny L.J., and Sarrieau A. The effects of neonatal handling on the development of the adrenocortical response to stress: implications for neuropathology and cognitive deficits in the later life. Psychoneuroendocrinology 16 (1991) 85-103
43. Meerlo P., Horvath K.M., Nagy G.M., Bohus B., and Koolhaas J.M. The influence of postnatal handling on adult neuroendocrine and behavioural stress reactivity. J Neuroendocrinol 11 (1999) 925-933
44. Merlio J.P., Ernfors P., Jaber M., and Persson H. Molecular cloning of rat trkC and distribution of cells expressing messenger RNAs for members of the trk family in the rat central nervous system. Neuroscience 51 (1992) 513-532
45. Mitchell J.B., Iny L.J., and Meaney M.J. The role of serotonin in the development and environmental regulation of type II corticosteroid receptor binding in rat hippocampus. Brain Res Dev Brain Res 55 (1990) 231-235
46. Niblock M.M., Brunso-Bechtold J.K., and Riddle D.R. Insulin-like growth factor I stimulates dendritic growth in primary somatosensory cortex. J Neurosci 20 (2000) 4165-4176
47. Norrholm S.D., and Ouimet C.C. Altered dendritic spine density in animal models of depression and in response to antidepressant treatment. Synapse 42 (2001) 151-163
48. Patterson S.L., Grover L.M., Schwartzkroin P.A., and Bothwell M. Neurotrophin expression in rat hippocampal slices: a stimulus paradigm inducing LTP in CA1 evokes increases in BDNF and NT-3 mRNAs. Neuron 9 (1992) 1081-1088
49. Pham T.M., Soderstrom S., Henriksson B.G., and Mohammed A.H. Effects of neonatal stimulation on later cognitive function and hippocampal nerve growth factor. Behav Brain Res 86 (1997) 113-120
50. Pollock G.S., and Frost D.O. Complexity in the modulation of neurotrophic factor mRNA expression by early visual experience. Brain Res Dev Brain Res 143 (2003) 225-232
51. Pryce C.R., Bettschen D., and Feldon J. Comparison of the effects of early handling and early deprivation on maternal care in the rat. Dev Psychobiol 38 (2001) 239-251
52. Pryce C.R., Bettschen D., Nanz-Bahr N.I., and Feldon J. Comparison of the effects of early handling and early deprivation on conditioned stimulus, context, and spatial learning and memory in adult rats. Behav Neurosci 117 (2003) 883-893
53. Saini H.S., Coelho R.P., Goparaju S.K., Jolly P.S., Maceyka M., Spiegel S., and Sato-Bigbee C. Novel role of sphingosine kinase 1 as a mediator of neurotrophin-3 action in oligodendrocyte progenitors. J Neurochem 95 (2005) 1298-1310
54. Saini H.S., Gorse K.M., Boxer L.M., and Sato-Bigbee C. Neurotrophin-3 and a CREB-mediated signaling pathway regulate Bcl-2 expression in oligodendrocyte progenitor cells. J Neurochem 89 (2004) 951-961
55. Shieh P.B., and Ghosh A. Molecular mechanisms underlying activity-dependent regulation of BDNF expression. Neurobiology 41 (1999) 127-134
56. Shieh P.B., Hu S.C., Bobb K., Timmusk T., and Ghosh A. Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron 20 (1998) 727-740
57. Soderstrom S., and Ebendal T. The levels of neurotrophin-3 protein in the rat brain determined by enzyme immunoassay show a pattern distinct from nerve growth factor. Neurosci Lett 189 (1995) 5-8
58. Tang A.C., and Zou B. Neonatal exposure to novelty enhances long-term potentiation in CA1 of the rat hippocampus. Hippocampus 12 (2002) 398-404
59. Torasdotter M., Metsis M., Henriksson B.G., Winblad B., and Mohammed A.H. Expression of neurotrophin-3 mRNA in the rat visual cortex and hippocampus is influenced by environmental conditions. Neurosci Lett 218 (1996) 107-110
60. van Oers H.J., de Kloet E.R., Whelan T., and Levine S. Maternal deprivation effect on the infant's neural stress markers is reversed by tactile stimulation and feeding but not by suppressing corticosterone. J Neurosci 18 (1998) 10171-10179
61. Wilson D.A., Willner J., Kurz E.M., and Nadel L. Early handling increases hippocampal long-term potentiation in young rats. Behav Brain Res 21 (1986) 223-227
62. Zhou X.E., and Rush R.A. Localization of neurotrophin-3-like immunoreactivity in the rat central nervous system. Brain Res 643 (1994) 162-172