Glucocorticoid signaling and exercise-induced downregulation of the mineralocorticoid receptor in the induction of adult mouse dentate neurogenesis by treadmill running

Psychoneuroendocrinology

Volumn 33, Issue 9, 2008, Pages 1173-1182

  Chang, Ya Ting ^a   Chen, Yi Chieh ^a   Wu, Chih Wei ^a   Yu, Lung ^a   Chen, Hsiun Ing ^a   Jen, Chauying J ^a   Kuo, Yu Min ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

Adrenalectomy; Adult neurogenesis; Corticosterone; Exercise; Mineralocorticoid receptor; Neuronal progenitor cells

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CITRATE SYNTHASE; CORTICOSTERONE; DOUBLECORTIN; GLUCOCORTICOID; MINERALOCORTICOID RECEPTOR; SPIRONOLACTONE;

ADRENALECTOMY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; DOWN REGULATION; ENZYME ACTIVITY; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL; TREADMILL EXERCISE;

ADRENALECTOMY; ADULT STEM CELLS; ANALYSIS OF VARIANCE; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DIFFERENTIATION; CORTICOSTERONE; DENTATE GYRUS; GENE EXPRESSION REGULATION; HORMONE ANTAGONISTS; MALE; MICE; MICE, INBRED C57BL; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; NEUROPEPTIDES; PHYSICAL CONDITIONING, ANIMAL; RECEPTOR, TRKB; RECEPTORS, MINERALOCORTICOID; RUNNING; SIGNAL TRANSDUCTION; SPIRONOLACTONE; STATISTICS, NONPARAMETRIC;

EID: 51249090505     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2008.05.014     Document Type: Article

References (55)

1. Abraham I., Veenema A.H., Nyakas C., Harkany T., Bohus B.G., and Luiten P.G. Effect of corticosterone and adrenalectomy on NMDA-induced cholinergic cell death in rat magnocellular nucleus basalis. J. Neuroendocrinol. 9 (1997) 713-720
2. Abraham I.M., Harkany T., Horvath K.M., and Luiten P.G. Action of glucocorticoids on survival of nerve cells: promoting neurodegeneration or neuroprotection?. J. Neuroendocrinol. 13 (2001) 749-760
3. Arriza J.L., Simerly R.B., Swanson L.W., and Evans R.M. The neuronal mineralocorticoid receptor as a mediator of glucocorticoid response. Neuron 1 (1988) 887-900
4. Avital A., Segal M., and Richter-Levin G. Contrasting roles of corticosteroid receptors in hippocampal plasticity. J. Neurosci. 26 (2006) 9130-9134
5. Benraiss A., Chmielnicki E., Lerner K., Roh D., and Goldman S.A. Adenoviral brain-derived neurotrophic factor induces both neostriatal and olfactory neuronal recruitment from endogenous progenitor cells in the adult forebrain. J. Neurosci. 21 (2001) 6718-6731
6. Black J.E., Isaacs K.R., Anderson B.J., Alcantara A.A., and Greenough W.T. Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc. Natl. Acad. Sci. U.S.A. 87 (1990) 5568-5572
7. Cameron H.A., and Gould E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61 (1994) 203-209
8. Cameron H.A., and McKay R.D. Restoring production of hippocampal neurons in old age. Nat. Neurosci. 2 (1999) 894-897
9. Cameron H.A., Woolley C.S., and Gould E. Adrenal steroid receptor immunoreactivity in cells born in the adult rat dentate gyrus. Brain Res. 611 (1993) 342-346
10. Carro E., Nunez A., Busiguina S., and Torres-Aleman I. Circulating insulin-like growth factor I mediates effects of exercise on the brain. J. Neurosci. 20 (2000) 2926-2933
11. Chao H.M., Ma L.Y., McEwen B.S., and Sakai R.R. Regulation of glucocorticoid receptor and mineralocorticoid receptor messenger ribonucleic acids by selective agonists in the rat hippocampus. Endocrinology 139 (1998) 1810-1814
12. Cotman C.W., and Berchtold N.C. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci. 25 (2002) 295-301
13. Davies C.T., and Few J.D. Effects of exercise on adrenocortical function. J. Appl. Physiol. 35 (1973) 887-891
14. Droste S.K., Gesing A., Ulbricht S., Muller M.B., Linthorst A.C., and Reul J.M. Effects of long-term voluntary exercise on the mouse hypothalamic-pituitary-adrenocortical axis. Endocrinology 144 (2003) 3012-3023
15. Escorihuela R.M., Tobena A., and Fernandez-Teruel A. Environmental enrichment and postnatal handling prevent spatial learning deficits in aged hypoemotional (Roman high-avoidance) and hyperemotional (Roman low-avoidance) rats. Learn. Mem. 2 (1995) 40-48
16. Fischer A.K., von Rosenstiel P., Fuchs E., Goula D., Almeida O.F., and Czeh B. The prototypic mineralocorticoid receptor agonist aldosterone influences neurogenesis in the dentate gyrus of the adrenalectomized rat. Brain Res. 947 (2002) 290-293
17. Fuller P.J., and Young M.J. Mechanisms of mineralocorticoid action. Hypertension 46 (2005) 1227-1235
18. Gage F.H. Mammalian neural stem cells. Science 287 (2000) 1433-1438
19. Garcia A., Steiner B., Kronenberg G., Bick-Sander A., and Kempermann G. Age-dependent expression of glucocorticoid- and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus. Aging Cell 3 (2004) 363-371
20. Gomes W.A., Mehler M.F., and Kessler J.A. Transgenic overexpression of BMP4 increases astroglial and decreases oligodendroglial lineage commitment. Dev. Biol. 255 (2003) 164-177
21. Gould E., Cameron H.A., Daniels D.C., Woolley C.S., and McEwen B.S. Adrenal hormones suppress cell division in the adult rat dentate gyrus. J. Neurosci. 12 (1992) 3642-3650
22. Gross R.E., Mehler M.F., Mabie P.C., Zang Z., Santschi L., and Kessler J.A. Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17 (1996) 595-606
23. Holmes M.C., French K.L., and Seckl J.R. Dysregulation of diurnal rhythms of serotonin 5-HT2C and corticosteroid receptor gene expression in the hippocampus with food restriction and glucocorticoids. J. Neurosci. 17 (1997) 4056-4065
24. Huang A.M., Jen C.J., Chen H.F., Yu L., Kuo Y.M., and Chen H.I. Compulsive exercise acutely upregulates rat hippocampal brain-derived neurotrophic factor. J. Neural Transm. 113 (2006) 803-811
25. Jacobsen J.P., and Mork A. Chronic corticosterone decreases brain-derived neurotrophic factor (BDNF) mRNA and protein in the hippocampus, but not in the frontal cortex, of the rat. Brain Res. 1110 (2006) 221-225
26. Kalman B.A., and Spencer R.L. Rapid corticosteroid-dependent regulation of mineralocorticoid receptor protein expression in rat brain. Endocrinology 143 (2002) 4184-4195
27. Kanagawa T., Tomimatsu T., Hayashi S., Shioji M., Fukuda H., Shimoya K., and Murata Y. The effects of repeated corticosteroid administration on the neurogenesis in the neonatal rat. Am. J. Obstet. Gynecol. 194 (2006) 231-238
28. Kaplan M.S., and Hinds J.W. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197 (1977) 1092-1094
29. Kretz O., Schmid W., Berger S., and Gass P. The mineralocorticoid receptor expression in the mouse CNS is conserved during development. Neuroreport 12 (2001) 1133-1137
30. Kronenberg G., Bick-Sander A., Bunk E., Wolf C., Ehninger D., and Kempermann G. Physical exercise prevents age-related decline in precursor cell activity in the mouse dentate gyrus. Neurobiol. Aging 27 (2006) 1505-1513
31. Kronenberg G., Reuter K., Steiner B., Brandt M.D., Jessberger S., Yamaguchi M., and Kempermann G. Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J. Comp. Neurol. 467 (2003) 455-463
32. Kwak S.P., Patel P.D., Thompson R.C., Akil H., and Watson S.J. 5′-Heterogeneity of the mineralocorticoid receptor messenger ribonucleic acid: differential expression and regulation of splice variants within the rat hippocampus. Endocrinology 133 (1993) 2344-2350
33. Li J., Ding Y.H., Rafols J.A., Lai Q., McAllister II J.P., and Ding Y. Increased astrocyte proliferation in rats after running exercise. Neurosci. Lett. 386 (2005) 160-164
34. Luger A., Deuster P.A., Gold P.W., Loriaux D.L., and Chrousos G.P. Hormonal responses to the stress of exercise. Adv. Exp. Med. Biol. 245 (1988) 273-280
35. McEwen B.S., De Kloet E.R., and Rostene W. Adrenal steroid receptors and actions in the nervous system. Physiol. Rev. 66 (1986) 1121-1188
36. Montaron M.F., Piazza P.V., Aurousseau C., Urani A., Le Moal M., and Abrous D.N. Implication of corticosteroid receptors in the regulation of hippocampal structural plasticity. Eur. J. Neurosci. 18 (2003) 3105-3111
37. Park E., Chan O., Li Q., Kiraly M., Matthews S.G., Vranic M., and Riddell M.C. Changes in basal hypothalamo-pituitary-adrenal activity during exercise training are centrally mediated. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289 (2005) R1360-R1371
38. Pencea V., Bingaman K.D., Wiegand S.J., and Luskin M.B. 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 (2001) 6706-6717
39. Ra S.M., Kim H., Jang M.H., Shin M.C., Lee T.H., Lim B.V., Kim C.J., Kim E.H., Kim K.M., and Kim S.S. Treadmill running and swimming increase cell proliferation in the hippocampal dentate gyrus of rats. Neurosci. Lett. 333 (2002) 123-126
40. Ratka A., Sutanto W., Bloemers M., and de Kloet E.R. On the role of brain mineralocorticoid (type I) and glucocorticoid (type II) receptors in neuroendocrine regulation. Neuroendocrinology 50 (1989) 117-123
41. Reul J.M., and de Kloet E.R. Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117 (1985) 2505-2511
42. Schaaf M.J., de Jong J., de Kloet E.R., and Vreugdenhil E. Downregulation of BDNF mRNA and protein in the rat hippocampus by corticosterone. Brain Res. 813 (1998) 112-120
43. Scharfman H., Goodman J., Macleod A., Phani S., Antonelli C., and Croll S. Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp. Neurol. 192 (2005) 348-356
44. Schefer V., and Talan M.I. Oxygen consumption in adult and aged C57BL/6J mice during acute treadmill exercise of different intensity. Exp. Gerontol. 31 (1996) 387-392
45. Schmiedek P., Sadee W., and Baethmann A. Cerebral uptake of a 3 H-labelled spirolactone compound in the dog. Eur. J. Pharmacol. 21 (1973) 238-241
46. Schreiber S.S., Sakhi S., Dugich-Djordjevic M.M., and Nichols N.R. Tumor suppressor p53 induction and DNA damage in hippocampal granule cells after adrenalectomy. Exp. Neurol. 130 (1994) 368-376
47. Sloviter R.S., Valiquette G., Abrams G.M., Ronk E.C., Sollas A.L., Paul L.A., and Neubort S. Selective loss of hippocampal granule cells in the mature rat brain after adrenalectomy. Science 243 (1989) 535-538
48. Soya H., Nakamura T., Deocaris C.C., Kimpara A., Iimura M., Fujikawa T., Chang H., McEwen B.S., and Nishijima T. BDNF induction with mild exercise in the rat hippocampus. Biochem. Biophys. Res. Commun. 358 (2007) 961-967
49. Stranahan A.M., Khalil D., and Gould E. Social isolation delays the positive effects of running on adult neurogenesis. Nat. Neurosci. 9 (2006) 526-533
50. Trejo J.L., Carro E., and Torres-Aleman I. Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J. Neurosci. 21 (2001) 1628-1634
51. van Praag H., Kempermann G., and Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 2 (1999) 266-270
52. van Praag H., Christie B.R., Sejnowski T.J., and Gage F.H. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 13427-13431
53. Wilson P.A., and Hemmati-Brivanlou A. Induction of epidermis and inhibition of neural fate by Bmp-4. Nature 376 (1995) 331-333
54. Wu C.W., Chen Y.C., Yu L., Chen H.I., Jen C.J., Huang A.M., Tsai H.J., Chang Y.T., and Kuo Y.M. Treadmill exercise counteracts the suppressive effects of peripheral lipopolysaccharide on hippocampal neurogenesis and learning and memory. J. Neurochem. 103 (2007) 2471-2481
55. Zigova T., Pencea V., Wiegand S.J., and Luskin M.B. Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol. Cell. Neurosci. 11 (1998) 234-245