Early maternal separation increases NGF expression in the developing rat hippocampus

Pharmacology Biochemistry and Behavior

Volumn 59, Issue 4, 1998, Pages 853-858

  Cirulli, Francesca ^a,b   Micera, Alessandra ^c   Alleva, Enrico ^a   Aloe, Luigi ^a,c  

^a Lab Fisiopatol Organo Sistema   (Italy)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Institute of Neurobiology   (Italy)

Author keywords

Development; Gene expression; Hippocampus; Maternal separation; NGF; Rat

Indexed keywords

MESSENGER RNA; NERVE GROWTH FACTOR; NEUROTROPHIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BORDERLINE STATE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPUS; MATERNAL DEPRIVATION; NERVE CELL DIFFERENTIATION; NEWBORN; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; RAT; SCHIZOPHRENIA;

ANIMALS; ANIMALS, NEWBORN; FEMALE; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MALE; MATERNAL DEPRIVATION; NERVE GROWTH FACTORS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER;

ANIMALIA; HIPPOCAMPUS HIPPOCAMPUS;

EID: 0032052202     PISSN: 00913057     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0091-3057(97)00512-1     Document Type: Article

References (46)

1. Ader R., Grota L. J. Effects of early experience on adrenocortical reactivity. Physiol. Behav. 4:1969;303-305.
2. Altman J., Das G. D., Anderson W. J. Effects of infantile handling on morphological development of the rat brain. An exploratory study Dev. Psychobiol. 1:1968;10-20.
3. Auberger G., Heumann R., Hellweg R., Korsching S., Thoenen H. I. Developmental changes of nerve growth factor and its mRNA in the hippocampus. Comparison with choline acetyltransferase Dev. Biol. 120:1987;223-328.
4. Bradley S. J. The relationship of early maternal separation to borderline personality disorder in children and adolescents. Am. J. Psychol. 136:1979;424-426.
5. Calamandrei G., Alleva E. Neuronal growth factors, neurotrophins and memory deficiency. Behav. Brain Res. 66:1995;129-132.
6. Calamandrei G., Valanzano A., Alleva E. NGF and cholinergic control of behavior. Anticipation and enhancement of scopolamine effects in neonatal mice Dev. Brain Res. 61:1991;237-241.
7. Coe C. L., Wiener S. G., Rosenberg L. T., Levine S. Physiological consequences of maternal separation and loss in the squirrel monkey. Rosenblum L. A., Coe C. L. Handbook of squirrel monkey research. 1985;127-148 Plenum Press, New York.
8. Crain B., Cotman C., Taylor D., Lynch G. A quantitative electron microscopic study of synaptogenesis in the dentate gyrus of the rat. Brain Res. 63:1973;195-204.
9. Field T. M., Schanberg S. M., Scafidi F., Bauer C. R., Vega-Lahr N., Garcia R., Nystrom J., Kuhn C. M. Effects of tactile/kinesthetic stimulation in pre-term neonates. Pediatrics. 77:1986;654-658.
10. Gall C. M., Isackson G. Limbic seizures increase neuronal production of messenger RNA for nerve growth factor. Science. 245:1989;758-761.
11. Gall C. M., Murray K., Isackson G. Kainic acid-induced seizures stimulate increased expression of nerve growth factor mRNA in rat hippocampus. Mol. Brain Res. 9:1991;113-123.
12. Gould E., Cameron H. A., Daniels D. C., Woolley C. S., McEwen B. S. Adrenal hormones suppress cell division in the adult rat dentate gyrus. J. Neurosci. 12:1992;3642-3650.
13. Gould E., Woolley C. S., McEwen B. S. The hippocampal formation. Morphological changes induced by thyroid, gonadal and adrenal hormones Psychoneuroendocrinology. 16:1991;67-84.
14. Grimes M. L., Zhou J., Beattie E. C., Yuen E. C., Hall D. E., Valletta J. S., Topp K. S., LaVail J. H., Bunnett N. W., Mobley W. C. Endocytosis of activated TrkA. Evidence that nerve growth factor induces formation of signaling endosomes J. Neurosci. 16:1996;7950-7964.
15. Hattori M., Nanko S. Association of neurotrophin-3 gene variant with severe forms of schizophrenia. Biochem. Biophys. Res. Commun. 209:1995;513-518.
16. Higley J. D., Suomi S. J., Linnoila M. A longitudinal assessment of CSF monoamine metabolite and plasma cortisol concentrations in young rhesus monkeys. Biol. Psychiat. 32:1992;127-145.
17. Hofer M. A. Relationships as regulators. A psychobiologic perspective on bereavement Psychosom. Med. 46:1984;183-197.
18. Jacobson S. Sequence of myelinization in the brain of the albino rat. Cerebral cortex, thalamus and related structures. J. Comp. Neurol. 121:1963;5-29.
19. Johnston M. V., Rutkowsky J. L., Wainer B. H., Long J. B., Mobley W. C. NGF effects on developing forebrain cholinergic neurons are regionally specific. Neurochem. Res. 12:1987;985-994.
20. Kuhn C. M., Butler S. R., Schanberg S. M. Selective depression of serum growth hormone during maternal deprivation in rat pups. Science. 201:1978;1034-1036.
21. Levine S. Infantile experience and resistance to physiological stress. Science. 126:1957;405-406.
22. Lindholm D., Heumann R., Meyer M., Thoenen H. Interleukin-1 regulates synthesis of nerve growth factor in non-neuronal cells of the rat sciatic nerve. Nature. 330:1987;658-659.
23. Lu B., Buck C. R., Dreyfus C. F., Black I. Expression of NGF and NGF receptor mRNAs in the developing brain. Evidence for local delivery and action of NGF Exp. Neurol. 104:1989;191-199.
24. McEwen B. S., Cameron H., Chao H. M., Gould E., Magarinos A., Yoshifumi W., Woolley C. S. Adrenal steroids and plasticity of hippocampal neurons. Toward an understanding of underlying cellular and molecular mechanisms Cell Mol. Neurobiol. 13:1993;457-482.
25. Meaney M. J., Aitken D. H., Bhatnagar S., Van Berkel C., Sapolsky R. M. Postnatal handling attenuates neuroendocrine, anatomical, and cognitive impairments related to the aged hippocampus. Science. 238:1988;766-768.
26. Mineka S., Suomi S. J. Social separation in monkeys. Psychol. Bull. 85:1978;1376-1400.
27. Mobley W. C., Rutkowsky J. L., Tennekoon G. I., Buchanan K., Johnston M. V. Choline acetyltransferase activity in striatum in neonatal rats increased by nerve growth factor. Science. 229:1985;284-287.
28. Mobley W. C., Rutkowsky J. L., Tennekoon G. I., Gemsky J., Buchanan K., Johnston M. V. Nerve growth factor increases choline acetyltransferase activity in developing basal forebrain neurons. Mol. Brain Res. 1:1986;53-62.
29. Mohammed A. K., Winblad B., Ebendal T., Larkfors L. Environmental influence on behavior and nerve growth factor in the brain. Brain Res. 528:1990;62-72.
30. Nadel L, Willner J. Some implications of postnatal maturation of the hippocampus. Chan-Palay V., Kohler C. The hippocampus. New vistas:1989;17-31 A. R. Liss, Inc, New York.
31. Rabizadeh S., Oh J., Zhong L., Yang J., Bitler C. M., Butcher L. L., Bredesen D. E. Induction of apoptosis by the low-affinity NGF receptor. Science. 261:1993;345-348.
32. Saffran B. N., Crutcher K. A. NGR-induced remodeling of mature uninjured axon collaterals. Brain Res. 525:1990;11-20.
33. Sapolsky R. M., Uno H., Rebert C. S., Finch C. E. Hippocampal damage associated with prolonged glucocorticoid exposure in primates. J. Neurosci. 10:1990;2897-2902.
34. Saugstad L. F. The maturational theory of brain development and cerebral excitability in the multifactorially inherited manic-depressive psychosis and schizophrenia. Int. J. Psychophysiol. 18:1994;189-203.
35. Sherwood N. M., Timiras P. S. A stereotaxic atlas of the developing brain. 1970;University of California Press, San Diego.
36. Spillantini M. G., Aloe L., Alleva E., De Simone R., Goedert M., Levi-Montalcini R. Nerve growth factor mRNA and protein increase in a mouse model of aggression. Proc. Natl. Acad. Sci. USA. 86:1989;8555-8559.
37. Suomi S. J., Harlow H. F. Production and alleviation of depressive behaviors in monkeys. Maser J., Seligman M. E. P. Psychopathology. Experimental models:1977;Freeman, San Francisco.
38. Sutula T., Ziao-Xian H., Cavazos J., Grayson S. Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science. 239:1988;1147-1150.
39. Tamborsky Harvey A., Moore H., Lucot J. B., Hennessy M. B. Monoamine activity in anterior hypothalamus of guinea pig pups separated from their mothers. Behav. Neurosci. 108:1994;171-176.
40. Vantini G., Schiavo N., Di Martino A., Polato P., Triban C., Callegaro L., Toffano G., Leon A. Evidence for a physiological role of nerve growth factor in the central nervous system of neonatal rats. Neuron. 3:1989;267-273.
41. Weskamp G., Otten U. An enzyme-linked immunoassay for nerve growth factor (NGF). A tool for studying regulatory mechanisms involved in NGF production in brain and peripheral tissues J. Neurochem. 48:1987;1779-1786.
42. Whittemore S. R., Ebendal T., Larkfors L., Olson L., Seiger A., Stromberg I., Persson H. Developmental and regional expression of β-nerve growth factor messenger RNA and protein in the rat central nervous system. Proc. Natl. Acad. Sci. USA. 83:1986;817-821.
43. Whittemore S. R., Friedman P. L., Larhammar D., Persson H., Gonzales-Carvajal M., Holets V. R. Rat β-nerve growth factor sequence and site of synthesis in the adult hippocampus. J. Neurosci. Res. 20:1988;403-410.
44. Wilson D. A., Willner J., Kurz E. M., Nadel L. Early handling increases hippocampal long-term potentiation in young rats. Behav. Brain Res. 21:1986;223-227.
45. Woolley C. S., Gould E., McEwen B. S. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res. 531:1990;225-231.
46. Zafra F., Hengerer B., Leibrock J., Thoenen H., Lindholm D. Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors. EMBO J. 9:1990;3545-3550.