Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus

European Journal of Neuroscience

Volumn 17, Issue 4, 2003, Pages 879-886

  Pham, Kara ^a,d   Nacher, Juan ^a,b   Hof, Patrick R ^c   McEwen, Bruce S ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF VALENCIA   (Spain)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d STANFORD UNIVERSITY   (United States)

Author keywords

Granule neuron; Hippocampus; Stereology

Indexed keywords

NERVE CELL ADHESION MOLECULE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL MATURATION; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; CHRONICITY; CONTROLLED STUDY; DENTATE GYRUS; GRANULE CELL; HIPPOCAMPUS; IMMOBILIZATION STRESS; MALE; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; RAT; TIME; UPREGULATION;

ANIMALS; BROMODEOXYURIDINE; CELL COUNT; CELL SURVIVAL; DENTATE GYRUS; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; MALE; NEURAL CELL ADHESION MOLECULE L1; NEURONS; PHOSPHOPYRUVATE HYDRATASE; RATS; RATS, SPRAGUE-DAWLEY; RESTRAINT, PHYSICAL; SIALIC ACIDS; STRESS; TIME FACTORS;

EID: 0037293553     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02513.x     Document Type: Article

References (53)

1. Bartolomucci, A., de Biurrun, G., Czeh, B., van Kampen, M. & Fuchs, E. (2002) Selective enhancement of spatial learning under chronic psychosocial stress. Eur. J. Neurosci., 15, 1863-1866.
2. Brezun, J.M. & Daszuta, A. (1999) Depletion in serotonin decreases neurogenesis in the dentate gyrus and the subventricular zone of adult rats. Neuroscience, 89, 999-1002.
3. Butler, A.K., Uryu, K. & Chesselet, M.F. (1998) A role for N-methyl-D-aspartate receptors in the regulation of synaptogenesis and expression of the polysialylated form of the neural cell adhesion molecule in the developing striatum. Dev. Neurosci., 20, 253-262.
4. Cameron, H.A. & Gould, E. (1994) Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience, 61, 203-209.
5. Cameron, H.A., McEwen, B.S. & Gould, E. (1995) Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J. Neurosci., 15, 4687-4692.
6. Cameron, H.A., Woolley, C.S., McEwen, B.S. & Gould, E. (1993) Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience, 56, 337-344.
7. Chattarji, S., Vyas, A., Mitra, R. & Rao, B.S.S. (2000) Effects of chronic unpredictable and immobilization stress on neuronal plasticity in the rat amygdala and hippocampus. Soc. Neurosci. Abstr., 26, 1533.
8. Conrad, C.D., Galea, L.A., Kuroda, Y. & McEwen, B.S. (1996) Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav. Neurosci., 110, 1321-1334.
9. Conrad, C.D., LeDoux, J.E., Magarinos, A.M. & McEwen, B.S. (1999) Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav. Neurosci., 113, 902-913.
10. Coughlan, C.M. & Breen, K.C. (1998) Glucocorticoid induction of the alpha2,6 sialyltransferase enzyme in a mouse neural cell line. J. Neurosci. Res., 51, 619-626.
11. Coughlan, C.M., Seckl, J.R, Fox, D.J., Unsworth, R. & Breen, K.C. (1996) Tissue-specific regulation of sialyltransferase activities in the rat by corticosteroids in vivo. Glycobiology, 6, 15-22.
12. Czeh, B., Michaelis, T., Watanabe, T., Frahm, J., de Biurrun, G., van Kampen, M., Bartolomucci, A. & Fuchs, E. (2001) Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc. Natl. Acad. Sci. USA, 98, 12796-12801.
13. Dellu, F., Mayo, W., Cherkaoui, J., Le Moal, M. & Simon, H. (1992) A two-trial memory task with automated recording: study in young and aged rats. Brain Res., 588, 132-139.
14. Gould, E. (1999) Serotonin and hippocampal neurogenesis. Neuropsychopharmacology, 21, 46S-51S.
15. Gould, E., Beylin, A., Tanapat, P., Reeves, A. & Shors, T.J. (1999) Learning enhances adult neurogenesis in the hippocampal formation. Nature Neurosci., 2. 260-265.
16. Gould, E., McEwen, B.S., Tanapat, P., Galea, L.A.M. & Fuchs, E. (1997) Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J. Neurosci., 17, 2492-2498.
17. Gould, E., Tanapat, P., McEwen, B.S., Flugge, G. & Fuchs, E. (1998) Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc. Natl. Acad. Sci. USA, 95, 3168-3171.
18. Kempermann, G., Kuhn, H.G. & Gage, F.H. (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature, 386, 493-495.
19. Kempermann, G., Kuhn, H.G. & Gage, F.H. (1998) Experience-induced neurogenesis in the senescent dentate gyrus. J. Neurosci., 18, 3206-3212.
20. Kiss, J.Z. & Rougon, G. (1997) Cell biology of polysialic acid. Curr. Opin. Neurobiol., 7, 640-646.
21. Lewis, P.D. (1978) Kinetics of cell proliferation in the postnatal rat dentate gyrus. Neuropathol. Appl. Neurobiol., 4, 191-195.
22. Luine, V., Martinez, C., Villegas, M., Magarinos, A.M. & McEwen, B.S. (1996) Restraint stress reversibly enhances spatial memory performance. Physiol. Behav., 59, 27-32.
23. Luine, V., Villegas, M, Martinez, C. & McEwen, B.S. (1994) Repeated stress causes reversible impairments of spatial memory performance. Brain Res., 639, 167-170.
24. Magarinos, A.M., Deslandes, A. & McEwen, B.S. (1999) Effects of antide-pressants and benzodiazepine treatments on the dendritic structure of CA3 pyramidal neurons after chronic stress. Eur. J. Pharmacol., 371, 113-122.
25. Magarinos, A.M. & McEwen, B.S. (1995) Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience, 69, 89-98.
26. Magarinos, A.M., McEwen, B.S., 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. Magarinos, A.M., Verdugo, J.M. & McEwen, B.S. (1997) Chronic stress alters synaptic terminal structure in hippocampus. Proc. Natl. Acad. Sci. USA, 94, 14002-14008.
28. Maguire, T.M., Coughlan, C.M., Seckl, J.R. & Breen, K.C. (1998) The effect of corticosteroids on serum sialyltransferase enzyme activities in the rat. Biochim. Biophys. Acta, 1379, 23-28.
29. Minturn, J.E., Geschwind, D.H., Fryer, H.J. & Hockfield, S. (1995) Early postmitotic neurons transiently express TOAD-64, a neural specific protein. J. Comp. Neurol., 355, 369-379.
30. Nacher, J., Alonso-Llosa, G., Rosell, D. & McEwen, B. (2002) PSA-NCAM expression in the piriform cortex of the adult rat. Modulation by NMDA receptor antagonist administration. Brain Res., 927, 111-121.
31. Nacher, J., Rosell, D.R., Alonso-Llosa, G. & McEwen, B.S. (2001) NMDA receptor antagonist treatment induces a long-lasting increase in the number of proliferating cells, PSA-NCAM-immunoreactive granule neurons and radial glia in the adult rat dentate gyrus. Eur. J. Neurosci., 13, 512-520.
32. Ohl, F. & Fuchs, E. (1999) Differential effects of chronic stress on memory processes in the tree shrew. Brain Res. Cogn. Brain Res., 7, 379-387.
33. Packard, D.S. Jr, Menzies, R.A. & Skalko, R.G. (1973) Incorporation of thymidine and its analogue, bromodeoxyuridine, into embryos and maternal tissues of the mouse. Differentiation, 1, 397-404.
34. van Praag, H., Christie, B.R., Sejnowski, T.J. & Gage, F.H. (1999a) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl. Acad. Sci. USA, 96, 13427-13431.
35. van Praag, H., Kempermann, G. & Gage, F.H. (1999b) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nature Neurosci., 2, 266-270.
36. Rodriguez, J.J., Montaron, M.F., Petty, K.G., Aurousseau, C., Marinelli, M., Premier, S., Rougon, G., Le Moal, M. & Abrous, D.N. (1998) Complex regulation of the expression of the polysialylated form of the neuronal cell adhesion molecule by glucocorticoids in the rat hippocampus. Eur. J. Neurosci., 10, 2994-3006.
37. Rougon, G., Dubois, C., Bucldey, N., Magnani, J.L. & Zollinger, W. (1986) A monoclonal antibody against meningococcus group B polysaccharides distinguishes embryonic from adult N-CAM. J. Cell Biol., 103, 2429-2437.
38. Sandi, C., Merino, J.J., Cordero, M.I., Touyarot, K. & Venero, C. (2001) Effects of chronic stress on contextual fear conditioning and the hippocampal expression of the neural cell adhesion molecule, its polysialylation, and L1. Neuroscience, 102, 329-339.
39. Sapolsky, R.M. (1996) Why stress is bad for your brain. Science, 273, 749-750.
40. Sapolsky, R.M., Krey, L.C. & McEwen, B.S. (1985) Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. J. Neurosci., 5, 1222-1227.
41. Seki, T. & Arai, Y. (1993) Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J. Neurosci., 13, 2351-2358.
42. Seki, T. & Arai, Y. (1999) Different polysialic acid-neural cell adhesion molecule expression patterns in distinct types of mossy fiber boutons in the adult hippocampus. J. Comp. Neurol., 410, 115-125.
43. Sheline, Y.I., Sanghavi, M., Mintun, M.A. & Gado, M.H. (1999) Depression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. J. Neurosci., 19, 5034-5043.
44. Sousa, N., Lukoyanov, N.V., Madeira, M.D., Almeida, O.F. & Paula-Barbosa, M.M. (2000) Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience, 97, 253-266.
45. Spigelman, I., Yan, X.X., Obenaus, A., Lee, E.Y., Wasterlain, C.G. & Ribak, C.E. (1998) Dentate granule cells form novel basal dendrites in a rat model of temporal lobe epilepsy. Neuroscience, 86, 109-120.
46. Starkman, M.N., Gebarski, S.S., Berent, S. & Schteingart, D.E. (1992) Hippocampal formation volume, memory dysfunction, and cortisol levels in patients with Cushing's syndrome. Biol. Psychiatry, 32, 756-765.
47. Tanapat, P., Hastings, N.B., Reeves, A.J. & Gould, E. (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci., 19, 5792-5801.
48. Uno, H., Tarara, R., Else, J.G., Suleman, M.A. & Sapolsky, R.M. (1989) Hippocampal damage associated with prolonged and fatal stress in primates. J. Neurosci., 9, 1705-1711.
49. Vyas, A., Mitra, R., Shankaranarayana Rao, B.S. & Chattarji, S. (2002) Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J. Neurosci., 22, 6810-6818.
50. Watanabe, Y., Gould, E. & McEwen, B.S. (1992) Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res., 588, 341-345.
51. West, M.J., Slomianka, L. & Gundersen, H.J. (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec., 231, 482-497.
52. Wood, G.E., Young, T.L., Reagan, L.P. & McEwen, B.S. (2003) Acute and chronic stress alter the incidence of social conflict in male rats. Hormones Behav., 43, in press.
53. Woolley, C.S., Gould, E. & McEwen, B.S. (1990) Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res., 531, 225-231.