Effects of voluntary running on plasma levels of neurotrophins, hippocampal cell proliferation and learning and memory in stressed rats

Neuroscience

Volumn 222, Issue , 2012, Pages 289-301

  Yau, S Y ^a,b   Lau, B W M ^a,b   Zhang, E D ^a,b   Lee, J C D ^a,b,c   Li, A ^a,b   Lee, T M C ^b,c   Ching, Y P ^a,b   Xu, A M ^a   So, K F ^a,b,d  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

^d JINAN UNIVERSITY   (China)

Author keywords

BDNF; Corticosterone; Hippocampal cell proliferation; IGF 1; Stress; Voluntary running

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; SOMATOMEDIN C;

ACUTE STRESS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CELL PROLIFERATION; CHRONIC STRESS; COGNITIVE DEFECT; CONTROLLED STUDY; DEPRESSION; LEARNING; MALE; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT; SPATIAL MEMORY; WEIGHT CHANGE;

ANIMALS; BODY WEIGHT; BRAIN-DERIVED NEUROTROPHIC FACTOR; BROMODEOXYURIDINE; CELL DIFFERENTIATION; CELL PROLIFERATION; FLUORESCENT ANTIBODY TECHNIQUE; HIPPOCAMPUS; HYDROCORTISONE; IMMUNOHISTOCHEMISTRY; INSULIN-LIKE GROWTH FACTOR I; LEARNING; MALE; MAZE LEARNING; MEMORY; NERVE GROWTH FACTORS; ORGAN SIZE; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; RUNNING; STRESS, PSYCHOLOGICAL; TASTE;

EID: 84865616488     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.07.019     Document Type: Article

References (58)

1. Abellan R., Ventura R., Pichini S., Di Giovannandrea R., Bellver M., Olive R., Pacifici R., Pascual J.A., Zuccaro P., Segura J. Effect of physical fitness and endurance exercise on indirect biomarkers of recombinant growth hormone misuse: insulin-like growth factor I and procollagen type III peptide. Int J Sports Med 2006, 27:976-983.
2. Banfi G., Marinelli M., Roi G.S., Colombini A., Pontillo M., Giacometti M., Wade S. Growth hormone and insulin-like growth factor I in athletes performing a marathon at 4000m of altitude. Growth Regul 1994, 4:82-86.
3. Barde Y.A. Neurotrophins: a family of proteins supporting the survival of neurons. Prog Clin Biol Res 1994, 390:45-56.
4. Bjornebekk A., Mathe A.A., Brene S. The antidepressant effect of running is associated with increased hippocampal cell proliferation. Int J Neuropsychopharmacol 2005, 8:357-368.
5. Blugeot A., Rivat C., Bouvier E., Molet J., Mouchard A., Zeau B., Bernard C., Benoliel J.J., Becker C. Vulnerability to depression: from brain neuroplasticity to identification of biomarkers. J Neurosci 2011, 31:12889-12899.
6. Carro E., Nunez A., Busiguina S., Torres-Aleman I. Circulating insulin-like growth factor I mediates effects of exercise on the brain. J Neurosci 2000, 20:2926-2933.
7. Clark P.J., Brzezinska W.J., Thomas M.W., Ryzhenko N.A., Toshkov S.A., Rhodes J.S. Intact neurogenesis is required for benefits of exercise on spatial memory but not motor performance or contextual fear conditioning in C57BL/6J mice. Neuroscience 2008, 155:1048-1058.
8. Cotman C.W., Berchtold N.C. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 2002, 25:295-301.
9. Cotman C.W., Berchtold N.C., Christie L.A. Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 2007, 30:464-472.
10. Duman R.S., Heninger G.R., Nestler E.J. A molecular and cellular theory of depression. Arch Gen Psychiatry 1997, 54:597-606.
11. Duman R.S., Monteggia L.M. A neurotrophic model for stress-related mood disorders. Biol Psychiatry 2006, 59:1116-1127.
12. Duncko R., Cornwell B., Cui L., Merikangas K.R., Grillon C. Acute exposure to stress improves performance in trace eyeblink conditioning and spatial learning tasks in healthy men. Learn Mem 2007, 14:329-335.
13. Dunn A.J., Swiergiel A.H. Effects of acute and chronic stressors and CRF in rat and mouse tests for depression. Ann N Y Acad Sci 2008, 1148:118-126.
14. Erickson K.I., Voss M.W., Prakash R.S., Basak C., Szabo A., Chaddock L., Kim J.S., Heo S., Alves H., White S.M., Wojcicki T.R., Mailey E., Vieira V.J., Martin S.A., Pence B.D., Woods J.A., McAuley E., Kramer A.F. Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci USA 2011, 108:3017-3022.
15. Ernst C., Olson A.K., Pinel J.P., Lam R.W., Christie B.R. Antidepressant effects of exercise: evidence for an adult-neurogenesis hypothesis?. J Psychiatry Neurosci 2006, 31:84-92.
16. Farmer J., Zhao X., van Praag H., Wodtke K., Gage F.H., Christie B.R. Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience 2004, 124:71-79.
17. 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.
18. Gould E., Tanapat P., McEwen B.S., Flugge G., Fuchs E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci USA 1998, 95:3168-3171.
19. Gregus A., Wintink A.J., Davis A.C., Kalynchuk L.E. Effect of repeated corticosterone injections and restraint stress on anxiety and depression-like behavior in male rats. Behav Brain Res 2005, 156:105-114.
20. Griffin E.W., Mullally S., Foley C., Warmington S.A., O'Mara S.M., Kelly A.M. Aerobic exercise improves hippocampal function and increases BDNF in the serum of young adult males. Physiol Behav 2011, 104:934-941.
21. Hartmann L., Singrun M.E. Study and evaluation of symbiontic phenomena in bacteria by means of the biocenosis simulator. Zentralbl Bakteriol Orig 1968, 207:403-409.
22. Hellsten J., Wennstrom M., Mohapel P., Ekdahl C.T., Bengzon J., Tingstrom A. Electroconvulsive seizures increase hippocampal neurogenesis after chronic corticosterone treatment. Eur J Neurosci 2002, 16:283-290.
23. Jacobsen J.P., 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 2006, 1110:221-225.
24. Johnson S.A., Fournier N.M., Kalynchuk L.E. Effect of different doses of corticosterone on depression-like behavior and HPA axis responses to a novel stressor. Behav Brain Res 2006, 168:280-288.
25. Klein A.B., Williamson R., Santini M.A., Clemmensen C., Ettrup A., Rios M., Knudsen G.M., Aznar S. Blood BDNF concentrations reflect brain-tissue BDNF levels across species. Int J Neuropsychopharmacol 2011, 14:347-353.
26. Knaepen K., Goekint M., Heyman E.M., Meeusen R. Neuroplasticity - exercise-induced response of peripheral brain-derived neurotrophic factor: a systematic review of experimental studies in human subjects. Sports Med 2010, 40:765-801.
27. Kovalchuk Y., Hanse E., Kafitz K.W., Konnerth A. Postsynaptic induction of BDNF-mediated long-term potentiation. Science 2002, 295:1729-1734.
28. Kraemer W.J., Aguilera B.A., Terada M., Newton R.U., Lynch J.M., Rosendaal G., McBride J.M., Gordon S.E., Hakkinen K. Responses of IGF-I to endogenous increases in growth hormone after heavy-resistance exercise. J Appl Physiol 1995, 79:1310-1315.
29. Lafenetre P., Leske O., Ma-Hogemeie Z., Haghikia A., Bichler Z., Wahle P., Heumann R. Exercise can rescue recognition memory impairment in a model with reduced adult hippocampal neurogenesis. Front Behav Neurosci 2010, 3:34.
30. Lau W.M., Qiu G., Helmeste D.M., Lee T.M., Tang S.W., So K.F. Corticosteroid decreases subventricular zone cell proliferation, which could be reversed by paroxetine. Restor Neurol Neurosci 2007, 25:17-23.
31. Marmigere F., Givalois L., Rage F., Arancibia S., Tapia-Arancibia L. Rapid induction of BDNF expression in the hippocampus during immobilization stress challenge in adult rats. Hippocampus 2003, 13:646-655.
32. Martinowich K., Manji H., Lu B. New insights into BDNF function in depression and anxiety. Nat Neurosci 2007, 10:1089-1093.
33. Molendijk M.L., Bus B.A., Spinhoven P., Penninx B.W., Kenis G., Prickaerts J., Voshaar R.O., Elzinga B.M. Serum levels of brain-derived neurotrophic factor in major depressive disorder: state-trait issues, clinical features and pharmacological treatment. Mol Psychiatry 2011, 16:1088-1095.
34. Rasmussen P., Brassard P., Adser H., Pedersen M.V., Leick L., Hart E., Secher N.H., Pedersen B.K., Pilegaard H. Evidence for a release of brain-derived neurotrophic factor from the brain during exercise. Exp Physiol 2009, 94:1062-1069.
35. Rasmusson A.M., Shi L., Duman R. Downregulation of BDNF mRNA in the hippocampal dentate gyrus after re-exposure to cues previously associated with footshock. Neuropsychopharmacology 2002, 27:133-142.
36. Schwarz A.J., Brasel J.A., Hintz R.L., Mohan S., Cooper D.M. Acute effect of brief low- and high-intensity exercise on circulating insulin-like growth factor (IGF) I, II, and IGF-binding protein-3 and its proteolysis in young healthy men. J Clin Endocrinol Metab 1996, 81:3492-3497.
37. Servatius R.J., Shors T.J. Exposure to inescapable stress persistently facilitates associative and nonassociative learning in rats. Behav Neurosci 1994, 108:1101-1106.
38. Sheline Y.I., Sanghavi M., Mintun M.A., Gado M.H. Depression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. J Neurosci 1999, 19:5034-5043.
39. Shors T.J. Acute stress rapidly and persistently enhances memory formation in the male rat. Neurobiol Learn Mem 2001, 75:10-29.
40. Shors T.J., Mathew P.R. NMDA receptor antagonism in the lateral/basolateral but not central nucleus of the amygdala prevents the induction of facilitated learning in response to stress. Learn Mem 1998, 5:220-230.
41. Sterner E.Y., Kalynchuk L.E. Behavioral and neurobiological consequences of prolonged glucocorticoid exposure in rats: relevance to depression. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34:777-790.
42. Stone E.A., Lin Y. An anti-immobility effect of exogenous corticosterone in mice. Eur J Pharmacol 2008, 580:135-142.
43. Tang S.W., Chu E., Hui T., Helmeste D., Law C. Influence of exercise on serum brain-derived neurotrophic factor concentrations in healthy human subjects. Neurosci Lett 2008, 431:62-65.
44. Toups M.S., Greer T.L., Kurian B.T., Grannemann B.D., Carmody T.J., Huebinger R., Rethorst C., Trivedi M.H. Effects of serum Brain Derived Neurotrophic Factor on exercise augmentation treatment of depression. J Psychiatr Res 2011, 45:1301-1306.
45. Trejo J.L., Carro E., 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 2001, 21:1628-1634.
46. Trejo J.L., Llorens-Martin M.V., Torres-Aleman I. The effects of exercise on spatial learning and anxiety-like behavior are mediated by an IGF-I-dependent mechanism related to hippocampal neurogenesis. Mol Cell Neurosci 2008, 37:402-411.
47. van Praag H., Christie B.R., Sejnowski T.J., Gage F.H. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 1999, 96:13427-13431.
48. van Praag H., Kempermann G., Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 1999, 2:266-270.
49. van Praag H., Shubert T., Zhao C., Gage F.H. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 2005, 25:8680-8685.
50. Vaynman S., Ying Z., Gomez-Pinilla F. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 2004, 20:2580-2590.
51. Wong E.Y., Herbert J. Raised circulating corticosterone inhibits neuronal differentiation of progenitor cells in the adult hippocampus. Neuroscience 2006, 137:83-92.
52. Yakar S., Liu J.L., Stannard B., Butler A., Accili D., Sauer B., LeRoith D. Normal growth and development in the absence of hepatic insulin-like growth factor I. Proc Natl Acad Sci USA 1999, 96:7324-7329.
53. Yau S.Y., Lau B.W., So K.F. Adult hippocampal neurogenesis: a possible way how physical exercise counteracts stress. Cell Transplant 2011, 20:99-111.
54. Yau S.Y., Lau B.W.M., Tong J.B., Ching Y.P., Lee T.M.C., So K.F. Hippocampal neurogenesis and dendritic plasticity support running-improved spatial learning and depression-like behaviour in stressed rats. PLos One 2011, 6:1-15.
55. Yau S.Y., Lee J.C.D., Lau B.W.M., Lee T.M.C., Ching Y.P., Tang S.W., So K.F. Low dose of corticosterone treatment with exercise increases hippocampal cell proliferation, and improves cognition. Neural Regen Res 2011, 6:2645-2655.
56. Zhao Y., Ma R., Shen J., Su H., Xing D., Du L. A mouse model of depression induced by repeated corticosterone injections. Eur J Pharmacol 2008, 581:113-120.
57. Zhao Y., Xie W., Dai J., Wang Z., Huang Y. The varying effects of short-term and long-term corticosterone injections on depression-like behavior in mice. Brain Res 2009, 1261:82-90.
58. Zheng H., Liu Y., Li W., Yang B., Chen D., Wang X., Jiang Z., Wang H., Wang Z., Cornelisson G., Halberg F. Beneficial effects of exercise and its molecular mechanisms on depression in rats. Behav Brain Res 2006, 168:47-55.