Time-course of hippocampal granule cell degeneration and changes in adult neurogenesis after adrenalectomy in rats

Neuroscience

Volumn 190, Issue , 2011, Pages 166-176

  Spanswick, S C ^a   Epp, J R ^a   Sutherland, R J ^a  

^a UNIVERSITY OF LETHBRIDGE   (Canada)

Author keywords

Cell death; Corticosterone; Dentate gyrus; Fluoro Jade B; Ki67; Proliferation

Indexed keywords

CORTICOSTERONE; KI 67 ANTIGEN;

ADRENALECTOMY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DEATH; CELL LABELING; CELL PROLIFERATION; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DENTATE GYRUS; GRANULE CELL; MALE; NERVE CELL DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RAT;

ADRENALECTOMY; ANIMALS; CELL COUNT; CELL DEATH; HIPPOCAMPUS; MALE; NERVE DEGENERATION; NEUROGENESIS; NEURONS; RATS; RATS, LONG-EVANS; TIME FACTORS;

EID: 80051585250     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.06.023     Document Type: Article

References (70)

1. Alahmed S., Herbert J. Strain differences in proliferation of progenitor cells in the dentate gyrus of the adult rat and the response to fluoxetine are dependent on corticosterone. Neuroscience 2008, 157:677-682.
2. Amrein I., Slomianka L., Lipp H.P. Granule cell number, cell death and cell proliferation in the dentate gyrus of wild-living rodents. Eur J Neurosci 2004, 20:3342-3350.
3. Anderson K.J., Fugaccia I., Scheff S.W. Fluoro-Jade B stains quiescent and reactive astrocytes in the rodent spinal cord. J Neurotrauma 2003, 20:1223-1231.
4. Andrés S., Cárdenas S., Parra C., Bravo J., Greiner M., Rojas P., Morales P., Lara H., Fiedler J. Effects of long-term adrenalectomy on apoptosis and neuroprotection in the rat hippocampus. Endocrine 2006, 29:299-307.
5. Boekhoorn K., Joëls M., Lucassen P.J. Increased proliferation reflects glial and vascular-associated changes, but not neurogenesis in the presenile Alzheimer hippocampus. Neurobiol Dis 2006, 24:1-14.
6. Brummelte S., Galea L.A. Chronic high corticosterone reduces neurogenesis in the dentate gyrus of adult male and female rats. Neuroscience 2010, 168:680-690.
7. Brunson K.L., Baram T.Z., Bender R.A. Hippocampal neurogenesis is not enhanced by lifelong reduction of glucocorticoid levels. Hippocampus 2005, 15:491-501.
8. Cameron H.A., Gould E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 1994, 61:203-209.
9. Cameron H.A., Gould E. Distinct populations of cells in the adult dentate gyrus undergo mitosis or apoptosis in response to adrenalectomy. J Comp Neurol 1996, 369:56-63.
10. Cameron H.A., Tanapat P., Gould E. Adrenal steroids and N-methyl-d-aspartate receptor activation regulate neurogenesis in the dentate gyrus of adult rats through a common pathway. Neuroscience 1998, 82:349-354.
11. Chauveau F., Tronche C., Piérard C., Liscua P., Drouet I., Coutan M., Béracochéa D. Rapid stress-induced corticosterone rise in the hippocampus reverses serial memory retrieval pattern. Hippocampus 2010, 20:196-207.
12. Conrad C.D., Roy E.J. Dentate gyrus destruction and spatial learning impairment after corticosteroid removal in young and middle-aged rats. Hippocampus 1995, 5:1-15.
13. Croft A.P., O'Callaghan M.J., Shaw S.G., Connolly G., Jacquot C., Little H.J. Effects of minor laboratory procedures, adrenalectomy, social defeat or acute alcohol on regional brain concentrations of corticosterone. Brain Res 2008, 1238:12-22.
14. Damjanac M., Rioux Bilan A., Barrier L., Pontcharraud R., Anne C., Hugon J., Page G. Fluoro-Jade B staining as useful tool to identify activated microglia and astrocytes in a mouse transgenic model of Alzheimer's disease. Brain Res 2007, 1128:40-49.
15. Dupret D., Fabre A., Döbrössy M.D., Panatier A., Rodríguez J.J., Lamarque S., Lemaire V., Oliet S.H.R., Piazza P.-V., Abrous D.N. Spatial learning depends on both the addition and removal of new hippocampal neurons. PLoS Biol 2007, 5:e214.
16. Encinas J.M., Vaahtokari A., Enikolopov G. Fluoxetine targets early progenitor cells in the adult brain. Proc Natl Acad Sci U S A 2006, 103:8233-8238.
17. Epp J.R., Galea L.A. Hippocampus-dependent strategy choice predicts low levels of cell proliferation in the dentate gyrus. Neurobiol Learn Mem 2009, 91:437-446.
18. Ferland C.L., Schrader L.A. Cage mate separation in pair-housed male rats evokes an acute stress corticosterone response. Neurosci Lett 2011, 489:154-158.
19. Fernandes A.M., Maurer-Morelli C.V., Campos C.B., Mello M.L., Castilho R.F., Langone F. Fluoro-Jade but not Fluoro-Jade B, stains non-degenerating cells in brain and retina of embryonic and neonatal rats. Brain Res 2004, 1:24-33.
20. 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 1992, 12:3642-3650.
21. Gould E., Tanapat P. Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat. Neuroscience 1997, 80:427-436.
22. Gould E., Woolley C.S., McEwen B.S. Short-term glucocorticoid manipulations affect neuronal morphology and survival in the adult dentate gyrus. Neuroscience 1990, 37:367-375.
23. Greiner M., Cárdenas S., Parra C., Bravo J., Avalos A.M., Parades A., Lara H.E., Fiedler J.L. Adrenalectomy regulates apoptotic-associated genes in rat hippocampus. Endocrine 2001, 15:323-333.
24. Huang G.-J., Herbert J. Stimulation of neurogenesis in the hippocampus of the adult rat by fluoxetine requires rhythmic change in corticosterone. Biol Psychiatry 2006, 59:619-624.
25. Jaarsma D., Postema F., Korf J. Time course and distribution of neuronal degeneration in the dentate gyrus of rat after adrenalectomy: a silver impregnation study. Hippocampus 1992, 2:143-150.
26. Jessberger S., Nakashima K., Clemenson G.D., Mejia E., Mathews E., Ure K., Ogawa S., Sinton C.M., Gage F.H., Hsieh J. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J Neurosci 2007, 27:5967-5975.
27. Jessberger S., Römer B., Babu H., Kempermann G. Seizures induce proliferation and dispersion of doublecortin-positive hippocampal progenitor cells. Exp Neurol 2005, 196:342-351.
28. Joëls M., Stienstra C., Karten Y. Effect of adrenalectomy on membrane properties and synaptic potentials in rat dentate granule cells. J Neurophysiol 2001, 85:699-707.
29. Karst H., Joëls M. Calcium currents in rat dentate granule cells are altered after adrenalectomy. Eur J Neurosci 2001, 14:503-512.
30. Kempermann G. Adult neurogenesis: stem cells and neuronal development in the adult brain 2006, Oxford University Press, New York.
31. Kempermann G., Gage F.H. Experience-dependent regulation of adult hippocampal neurogenesis: effects of long-term stimulation and stimulus withdrawal. Hippocampus 1999, 9:321-332.
32. Krause E.G., Sakai R.R. Richter and sodium appetite: from adrenalectomy to molecular biology. Appetite 2007, 49:353-367.
33. Krugers H.J., van der Linden S., van Olst E., Alfarez D.N., Maslam S., Lucassen P.J., Joëls M. Dissociation between apoptosis, neurogenesis, and synaptic potentiation in the dentate gyrus of adrenalectomized rats. Synapse 2007, 61:221-230.
34. Kundrotiene J., Wagner A., Liljequist S. Fluoro-Jade and TUNEL staining as useful tools to identify ischemic brain damage following moderate extradural compression of sensorimotor cortex. Acta Neurobiol Exp 2004, 64:153-162.
35. Lee C., Agoston D.V. Inhibition of VEGF receptor 2 increased cell death of dentate hilar neurons after traumatic brain injury. Exp Neurol 2009, 220:400-403.
36. Malberg J.E., Duman R.S. Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 2003, 28:1562-1571.
37. Malberg J.E., Eisch A.J., Nestler E.J., Duman R.S. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 2000, 20:9104-9110.
38. Mayer J.L., Klumpers L., de Kloet E.R., Joëls M., Lucassen P.J. Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the corticosterone-induced reduction of adult hippocampal neurogenesis. J Neuroendocrinol 2006, 18:629-631.
39. Melvin N.R., Sutherland R.J. Quantitative caveats of standard immunohistochemical procedures: implications for optical dissector-based designs. J Histochem Cytochem 2010, 58:577-584.
40. Montaron M.F., Petry K.G., Rodriguez J.J., Marinelli M., Aurousseau C., Rougon G., Le Moal M., Abrous D.N. Adrenalectomy increases neurogenesis but not PSA-NCAM expression in the aged dentate gyrus. Eur J Neurosci 1999, 11:1479-1485.
41. Moon J.B., Lee C.H., Park C.W., Cho J.H., Hwang I.K., Yoo K.Y., Choi J.H., Shin H.C., Won M.H. Neuronal degeneration and microglial activation in the ischemic dentate gyrus of the gerbil. J Vet Med Sci 2009, 71:1381-1386.
42. Mouton P.R. Principles and practices of unbiased stereology: an introduction for bioscientists 2002, The Johns Hopkins University Press, Baltimore.
43. Nair S.M., Karst H., Dumas T., Phillips R., Sapolsky R.M., Rumpff-van Essen L., Maslam S., Lucassen P.J., Joëls M. Gene expression profiles associated with survival of individual rat dentate cells after endogenous corticosteroid deprivation. Eur J Neurosci 2004, 20:3233-3243.
44. Naylor A.S., Persson A.I., Eriksson P.S., Jonsdottir I.H., Thorlin T. Extended voluntary running inhibits exercise-induced adult hippocampal progenitor proliferation in the spontaneously hypertensive rat. J Neurophysiol 2005, 93:2406-2414.
45. Park C., Kang M., Kim-Kwon Y., Kim J., Ahn H., Huh Y. Inhibition of neuronal nitric oxide synthase increases adrenalectomy-induced granule cell death in the rat dentate gyrus. Brain Res 2002, 933:81-84.
46. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, New York.
47. Pitkänen A., Nissinen J., Nairismägi J., Lukasiuk K., Gröhn O.H., Miettinen R., Kauppinen R. Progression of neuronal damage after status epilepticus and during spontaneous seizures in a rat model of temporal lobe epilepsy. Prog Brain Res 2002, 135:67-83.
48. Qin Y., Nair S., Karst H., Vreugdenhil E., Datson N., Joëls M. Gene expression changes in single dentate granule neurons after adrenalectomy of rats. Brain Res Mol Brain Res 2003, 111:17-23.
49. Rao M.S., Hattiangady B., Reddy D.S., Shetty A.K. Hippocampal neurodegeneration, spontaneous seizures, and mossy fiber sprouting in the F344 rat model of temporal lobe epilepsy. J Neurosci Res 2006, 83:1088-1105.
50. Roozendaal B., Sapolsky R.M., McGaugh J.L. Basolateral amygdala lesions block the disruptive effects of long-term adrenalectomy on spatial memory. Neuroscience 1998, 84:453-465.
51. Sahay A., Hen R. Adult hippocampal neurogenesis in depression. Nat Neurosci 2007, 10:1110-1115.
52. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., Weisstaub N., Lee J., Duman R., Arancio O., Belzung C., Hen R. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003, 301:805-809.
53. Sapolsky R.M., Krey L.C., McEwen B.S. Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc Natl Acad Sci U S A 1984, 81:6174-6177.
54. Schlessinger A.R., Cowan W.M., Gottlieb D.I. An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J Comp Neurol 1975, 159:149-175.
55. Schmued L.C., Hopkins K.J. Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 2000, 874:123-130.
56. Scholzen T., Gerdes J. The Ki-67 protein: from the known and the unknown. J Cell Physiol 2000, 182:311-322.
57. Sloviter R.S., Sollas A.L., Neubort S. Hippocampal dentate granule cell degeneration after adrenalectomy in the rat is not reversed by dexamethasone. Brain Res 1995, 682:227-230.
58. Sloviter R.S., Valiquette G., Abrams G.M., Ronk E.C., Sollas A.L., Paul L.A., Neubort S. Selective loss of hippocampal granule cells in the mature rat brain after adrenalectomy. Science 1989, 243:535-538.
59. Smriga M., Saito H., Nishiyama N. Hippocampal long- and short-term potentiation is modulated by adrenalectomy and corticosterone. Neuroendocrinology 1996, 64:35-41.
60. Sousa N., Madeira M.D., Paula-Barbosa M.M. Structural alterations of the hippocampal formation of adrenalectomized rats: an unbiased stereological study. J Neurocytol 1997, 26:423-438.
61. Spanswick S.C., Bray D., Zelinski E.L., Sutherland R.J. A novel method for reliable nuclear antibody detection in tissue with high levels of pathology-induced autofluorescence. J Neurosci Methods 2009, 185:45-49.
62. Spanswick S.C., Epp J.R., Keith J.R., Sutherland R.J. Adrenalectomy-induced granule cell degeneration in the hippocampus causes spatial memory deficits that are not reversed by chronic treatment with corticosterone or fluoxetine. Hippocampus 2007, 17:137-146.
63. Spanswick S.C., Lehmann H., Sutherland R.J. A novel animal model of hippocampal cognitive deficits, slow neurodegeneration and neuroregeneration. J Biomed Biotechnol 2011, 2011:527201. 10.1155/2011/527201.
64. Spanswick S.C., Sutherland R.J. Object/context specific memory deficits associated with loss of hippocampal granule cells after adrenalectomy in rats. Learn Mem 2010, 17:241-245.
65. Stratmann G., Sall J.W., May L.D.V., Bell J.S., Magnusson K.R., Rau V., Visrodia K.H., Alvi R.S., Ku B., Lee M.T., Dai R. Isoflurane differentially affects neurogenesis and long-term neurocognitive function in 60-day-old and 7-day-old rats. Anesthesiology 2009, 110:834-848.
66. Wagner D.-C., Riegelsberger U.M., Michalk S., Härtig W., Kranz A., Boltze J. Cleaved caspase-3 expression after experimental stroke exhibits different phenotypes and is predominantly non-apoptotic. Brain Res 2011, 1381:237-242.
67. West M.J., Slomianka L., Gundersen H.J. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 1991, 231:482-497.
68. Wines-Samuelson M., Schulte E.C., Smith M.J., Aoki C., Liu X. Characterization of age-dependent and progressive cortical neuronal degeneration in presenilin conditional mutant mice. PLoS One 2010, 5:e101095. 10.1371/journal.pone.0010195.
69. Wong E.Y.H., Herbert J. Roles of mineralocorticoid and glucocorticoid receptors in the regulation of progenitor proliferation in the adult hippocampus. Eur J Neurosci 2005, 22:785-792.
70. Woolley C.S., Gould E., Sakai R.R., Spencer R.L., McEwen B.S. Effects of aldosterone or RU28362 treatment on adrenalectomy-induced cell death in the dentate gyrus of the adult rat. Brain Res 1991, 554:312-315.