Extended voluntary running inhibits exercise-induced adult hippocampal progenitor proliferation in the spontaneously hypertensive rat

Journal of Neurophysiology

Volumn 93, Issue 5, 2005, Pages 2406-2414

  Naylor, Andrew S ^a,b   Persson, Anders I ^c   Eriksson, Peter S ^c   Jonsdottir, Ingibjörg H ^a,d   Thorlin, Thorleif ^b  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b Institute of Clinical Neuroscience   (Sweden)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

^d Institute of Stress Medicine   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; CORTICOSTERONE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN;

ADRENAL GLAND; ANALYSIS OF VARIANCE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DENTATE GYRUS; DOWN REGULATION; EXERCISE; FEMALE; HIPPOCAMPUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOHISTOCHEMISTRY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RAT; RUNNING; SPONTANEOUSLY HYPERTENSIVE RAT; STEM CELL; STRESS; THYMUS; VOLUNTARY MOVEMENT;

ADRENAL GLANDS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BROMODEOXYURIDINE; CELL COUNT; CELL PROLIFERATION; CORTICOSTERONE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INHIBITION (PSYCHOLOGY); PHOSPHORYLATION; PHYSICAL CONDITIONING, ANIMAL; RANDOM ALLOCATION; RATS; RATS, INBRED SHR; RUNNING; STEM CELLS; THYMUS GLAND; TIME FACTORS;

EID: 17644413209     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.01085.2004     Document Type: Article

References (48)

1. Aberg MA, Aberg ND, Hedbacker H, Oscarsson J, and Eriksson PS. Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. J Neurosci 20: 2896-2903, 2000.
2. Akana SF, Cascio CS, Shinsako J, and Dallman MF. Corticosterone: narrow range required for normal body and thymus weight and ACTH. Am J Physiol 249: R527-R532, 1985.
3. Altman J and Das GD. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124: 319-335, 1965.
4. Brown ES, Rush AJ, and McEwen BS. Hippocampal remodeling and damage by corticosteroids: implications for mood disorders. Neuropsychopharmacology 21: 474-484, 1999.
5. Cameron HA and Gould E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61: 203-209, 1994.
6. Cameron HA, Woolley CS, and Gould E. Adrenal steroid receptor immunoreactivity in cells born in the adult rat dentate gyrus. Brain Res 611: 342-346, 1993.
7. Carro E, Trejo JL, Busiguina S, and Torres-Aleman I. Circulating insulin-like growth factor 1 mediates the protective effects of physical exercise against brain insults of different etiology and anatomy. J Neurosci 21: 5678-5684, 2001.
8. Coggeshall RE and Lekan HA. Methods for determining numbers of cells and synapses: a case for more uniform standards of review. J Comp Neurol 364: 6-15, 1996.
9. Cohen JJ. Glucocorticoid-induced apoptosis in the thymus. Semin Immunol 4: 363-369, 1992.
10. Concordet JP and Ferry A. Physiological programmed cell death in thymocytes is induced by physical stress (exercise). Am J Physiol 265: C626-C629, 1993.
11. Droste SK, Gesing A, Ulbricht S, Muller MB, Linthorst AC, and Reul JM. Effects of long-term voluntary exercise on the mouse hypothalamic-pituitary- adrenocortical axis. Endocrinology 144: 3012-3023, 2003.
12. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, and Gage FH. Neurogenesis in the adult human hippocampus. Nat Med 4: 1313-1317, 1998.
13. Eriksson PS and Wallin L. Functional consequences of stress-related suppression of adult hippocampal neurogenesis - a novel hypothesis on the neurobiology of burnout. Acta Neural Scand 110: 275-280, 2004.
14. Fabel K, Tam B, Kaufer D, Baiker A, Simmons N, Kuo CJ, and Palmer TD. VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci 18: 2803-2812, 2003.
15. Farmer J, Zhao X, Van Praag H, Wodtke K, Gage FH, and Christie BR. Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience 124: 71-79, 2004.
16. Gage FH, Kempermann G, Palmer TD, Peterson DA, and Ray J. Multipotent progenitor cells in the adult dentate gyrus. J Neurobiol 36: 249-266, 1998.
17. Gomez F, Lahmame A, de Kloet ER, and Armario A. Hypothalamic-pituitary- adrenal response to chronic stress in five inbred rat strains: differential responses are mainly located at the adrenocortical level. Neuroendocrinology 63: 327-337, 1996.
18. Gomez-Pinilla F, Ying Z, Roy RR, Molteni R, and Edgerton VR. Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity. J Neurophysiol 88: 2187-2195, 2002.
19. Gould E, Beylin A, Tanapat P, Reeves A, and Shors TJ. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2: 260-265, 1999.
20. Gould E, Cameron HA, Daniels DC, Woolley CS, and McEwen BS. Adrenal hormones suppress cell division in the adult rat dentate gyrus. J Neurosci 12: 3642-3650, 1992.
21. Gould E and McEwen BS. Neuronal birth and death. Curr Opin Neurobiol 3: 676-682, 1993.
22. Gould E, Tanapat P, Rydel T, and Hastings N. Regulation of hippocampal neurogenesis in adulthood. Biol Psychiatry 48: 715-720, 2000.
23. Gundersen HJ, Bendtsen TF, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sorensen FB, Vesterby A, and West MJ. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. Apmis 96: 379-394, 1988.
24. Holmes MM, Galea LA, Mistlberger RE, and Kempermann G. Adult hippocampal neurogenesis and voluntary running activity: circadian and dose-dependent effects. J Neurosci Res 76: 216-222, 2004.
25. Hori T, Fukuda M, Suzuki H, Yano S, and Ono T. SART stress effects on lymphocytes in the thymus and spleen of normal, adrenalectomized, and sympathectomized mice. Clin Immunol Immunopathol 68: 243-245, 1993.
26. Jacobs BL, Praag H, and Gage FH. Adult brain neurogenesis and psychiatry: a novel theory of depression. Mol Psychiatry 5: 262-269, 2000.
27. Jonsdottir IH and Hoffmann P. The significance of intensity and duration of exercise on natural immunity in rats. Med Sci Sports Exerc 32: 1908-1912, 2000.
28. Kent S, Hurd M, and Satinoff E. Interactions between body temperature and wheel running over the estrous cycle in rats. Physiol Behav 49: 1079-1084, 1991.
29. Kim JJ and Diamond DM. The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 3: 453-462, 2002.
30. McEwen BS, Gould EA, and Sakai RR. The vulnerability of the hippocampus to protective and destructive effects of glucocorticoids in relation to stress. Br J Psychiatry Suppl 15: 18-23, 1992.
31. Moraska A, Deak T, Spencer RL, Roth D, and Fleshner M. Treadmill running produces both positive and negative physiological adaptations in Sprague-Dawley rats. Am J Physiol Regul Integr Comp Physiol 279: R1321-R1329, 2000.
32. Nakagawa S, Kim JE, Lee R, Chen J, Fujioka T, Malberg J, Tsuji S, and Duman RS. Localization of phosphorylated cAMP response element-binding protein in immature neurons of adult hippocampus. J Neurosci 22: 9868-9876, 2002a.
33. Nakagawa S, Kim JE, Lee R, Malberg JE, Chen J, Steffen C, Zhang YJ, Nestler EJ, and Duman RS. Regulation of neurogenesis in adult mouse hippocampus by cAMP and the cAMP response element-binding protein. J Neurosci 22: 3673-3682, 2002b.
34. Neeper SA, Gomez-Pinilla F, Choi J, and Cotman CW. Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res 726: 49-56, 1996.
35. Persson AI, Naylor AS, Jonsdottir IH, Nyberg F, Eriksson PS, and Thorlin T. Differential regulation of hippocampal progenitor proliferation by opioid receptor antagonists in running and non-running spontaneously hypertensive rats. Eur J Neurosci 19: 1847-1855, 2004.
36. Reul JM, Bilang-Bleuel A, Droste S, Linthorst AC, Holsboer F, and Gesing A. New mode of hypothalamic-pituitary-adrenocortical axis regulation: significance for stress-related disorders. Z Rheumatol 59(Suppl 2): 22-25, 2000.
37. Rhodes JS, van Praag H, Jeffrey S, Girard I, Mitchell GS, Garland T Jr, and Gage FH. Exercise increases hippocampal neurogenesis to high levels but does not improve spatial learning in mice bred for increased voluntary wheel running. Behav Neurosci 117: 1006-1016, 2003.
38. Rodriguez JJ, Montaron MF, Petry KG, Aurousseau C, Marinelli M, Premier S, Rougon G, Le Moal M, and Abrous DN. 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, 1998.
39. Sardessai SR, Abraham ME, and Mascarenhas JF. Effect of stress on organ weight in rats. Ind J Physiol Pharmacol 37: 104-108, 1993.
40. Shapiro M. Plasticity, hippocampal place cells, and cognitive maps. Arch Neurol 58: 874-881, 2001.
41. Sheline YI, Wang PW, Gado MH, Csernansky JG, and Vannier MW. Hippocampal atrophy in recurrent major depression. Proc Natl Acad Sci USA 93: 3908-3913, 1996.
42. Tong L, Shen H, Perreau VM, Balazs R, and Cotman CW. Effects of exercise on gene-expression profile in the rat hippocampus. Neurobiol Dis 8: 1046-1056, 2001.
43. Trejo JL, 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: 1628-1634, 2001.
44. van Praag H, Christie BR, Sejnowski TJ, and Gage FH. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96: 13427-13431, 1999a.
45. van Praag H, Kempermann G, and Gage FH. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2: 266-270, 1999b.
46. Yamamoto T, Ohkuwa T, Itoh H, Sato Y, and Naoi M. Relation between voluntary physical activity and oxidant/antioxidant status in rats. Comp Biochem Physiol C Toxicol Pharmacol 135: 163-168, 2003.
47. Yehuda R, Fairman KR, and Meyer JS. Enhanced brain cell proliferation following early adrenalectomy in rats. J Neurochem 53: 241-248, 1989.
48. Yu IT, Lee SH, Lee YS, and Son H. Differential effects of corticosterone and dexamethasone on hippocampal neurogenesis in vitro. Biochem Biophys Res Commun 317: 484-490, 2004.