Exercise activates the phosphatidylinositol 3-kinase pathway

Molecular Brain Research

Volumn 135, Issue 1-2, 2005, Pages 181-193

  Chen, Michael J ^a   Russo Neustadt, Amelia A ^a  

^a CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

BDNF; CREB; Physical activity; Signaling; Western blotting

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; BRAIN DERIVED NEUROTROPHIC FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOGLYCOGEN SYNTHASE KINASE 3BETA; PHOSPHOSERINE; PHOSPHOTHREONINE; PROTEIN KINASE B; SODIUM CHLORIDE; TRANYLCYPROMINE; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; EXERCISE; EXPERIMENTAL TEST; HIPPOCAMPUS; IMMUNOBLOTTING; INTERMETHOD COMPARISON; MALE; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RUNNING; SITTING; STATISTICAL SIGNIFICANCE; TREADMILL;

ANIMALIA;

EID: 18044394417     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbrainres.2004.12.001     Document Type: Article

References (137)

1. D.R. Alessi, S.R. James, C.P. Downes, A.B. Holmes, P.R. Gaffney, C.B. Reese, and P. Cohen Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase B alpha Curr. Biol. 7 1997 261 269
2. R. Aloyz, J.P. Fawcett, D.R. Kaplan, R.A. Murphy, and F.D. Miller Activity-dependent activation of trkB neurotrophin receptors in the adult CNS Learn. Mem. 6 1999 216 231
3. C.A. Altar Neurotrophins and depression Trends Pharmacol. Sci. 20 1999 59 61
4. 1A-adrenergic receptor J. Biol. Chem. 276 2001 40910 40916
5. F. Barnabé-Heider, and F.D. Miller Endogenously produced neurotrophins regulate survival and differentiation of cortical progenitors via distinct signaling pathways J. Neurosci. 23 2003 5149 5160
6. G.T. Baxter, M.J. Radeke, R.C. Kuo, V. Makrides, B. Hinkle, R. Hoang, A. Medina-Selby, D. Coit, P. Valenzuela, and S.C. Feinstein Signal transduction mediated by the truncated trkB receptor isoforms, trkB.T1 and trkB.T2 J. Neurosci. 17 1997 2683 2690
7. M.M. Behrens, U. Strasser, J.-Y. Koh, B.J. Gwag, and D.W. Choi Prevention of neuronal apoptosis by phorbol ester-induced activation of protein kinase c: blockade of p38 mitogen-activated protein kinase Neuroscience 94 1999 917 927
8. N.C. Berchtold, H.S. Oliff, P. Isaxkson, and C.W. Cotman Brain-derived neurotrophic factor (BDNF) shows a circadian pattern of expression in the hippocampal formation Abstr.-Soc. Neurosci. 23 1997 46
9. S.V. Bhave, L. Ghoda, and P.L. Hoffman Brain-derived neurotrophic factor mediates the anti-apoptotic effect of NMDA in cerebellar granule neurons: signal transduction cascades and site of ethanol action J. Neurosci. 19 1999 3277 3286
10. D.K. Binder, M.J. Routbort, and J.O. McNamara Immunohistochemical evidence of seizure-induced activation of trk receptors in the mossy fiber pathway of adult rat hippocampus J. Neurosci. 19 1999 4616 4626
11. P.R. Blanquet Identification of two persistently activated neurotrophin-regulated pathways in rat hippocampus Neuroscience 95 1999 705 719
12. 2+/calmodulin-dependent protein kinase 2 activity in hippocampus J. Biol. Chem. 272 1997 24133 24136
13. P.R. Blanquet, J. Mariani, and P. Derer A calcium/calmodulin kinase pathway connects brain-derived neurotrophic factor to the cyclic AMP-responsive transcription factor in the rat hippocampus Neuroscience 118 2003 477 490
14. K. Brami-Cherrier, E. Valjent, M. Garcia, C. Pages, R.A. Hipskind, and J. Caboche Dopamine induces a PI3-kinase-independent activation of Akt in striatal neurons: a new route to cAMP response element-binding protein phosphorylation J. Neurosci. 22 2002 8911 8921
15. A. Brunet, A. Bonni, M.J. Zigmond, M.Z. Lin, P. Juo, L.S. Hu, M.J. Anderson, K.C. Arden, J. Blenis, and M.E. Greenberg Akt promotes cell survival by phosphorylating and inhibiting a forkhead transcription factor Cell 96 1999 857 868
16. A. Brunet, S.R. Datta, and M.E. Greenberg Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway Curr. Opin. Neurobiol. 11 2001 297 305
17. B.M.Th. Burgering, and P.J. Coffer Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction Nature 376 1995 599 602
18. M.H. Cardone, N. Roy, H.R. Stennicke, G.S. Salvesen, T.F. Franke, E. Stanbridge, S. Frisch, and J.C. Reed Regulation of cell death protease caspase-9 by phosphorylation Science 282 1998 1318 1321
19. E. Castrén, B. Berninger, A. Leingärtner, and D. Lindholm Regulation of brain-derived neurotrophic factor mRNA levels in hippocampus by neuronal activity Prog. Brain Res. 117 1998 57 64
20. T.O. Chan, S.E. Rittenhouse, and P.N. Tsichlis AKT/PKB and other D3 phosphoinositide-regulated kinases: kinase activation by phosphoinositide- dependent phosphorylation Annu. Rev. Biochem. 68 1999 965 1014
21. A.C.-H. Chen, Y. Shirayama, K.-H. Shin, R.L. Neve, and R.S. Duman Expression of the cAMP response element binding protein (CREB) in hippocampus produces an antidepressant effect Biol. Psychiatry 49 2001 753 762
22. Y.H. Chung, E.J. Kim, C.M. Shin, K.M. Joo, M.J. Kim, H.W. Woo, and C.I. Cha Age-related changes in CREB binding protein immunoreactivity in the cerebral cortex and hippocampus of rats Brain Res. 956 2002 312 318
23. A.C. Conti, J.F. Cryan, A. Dalvi, I. Lucki, and J.A. Blendy cAMP response element-binding protein is essential for the upregulation of brain-derived neurotrophic factor transcription, but not the behavioral or endocrine responses to antidepressant drugs J. Neurosci. 22 2002 3262 3268
24. C.W. Cotman, and N.C. Berchtold Exercise: a behavioral intervention to enhance brain health and plasticity Trends Neurosci. 25 2002 295 301
25. D.A.E. Cross, D.R. Alessi, P. Cohen, M. Andjelkovich, and B.A. Hemmings Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B Nature 378 1995 785 789
26. T.G. Cross, D. Scheel-Toellner, N.V. Henriques, E. Deacon, M. Salmon, and J.M. Lord Serine/thronine protein kinases and apoptosis Exp. Cell Res. 256 2000 34 41
27. R.J. Crowder, and R.S. Freeman Glycogen synthase kinase-3β activity is critical for neuronal death caused by inhibiting phosphatidylinositol 3-kinase or Akt but not for death caused by nerve growth factor withdrawal J. Biol. Chem. 275 2000 34266 34271
28. H. Cui, Y. Meng, and R.F. Bulleit Inhibition of glycogen synthase 3β activity regulates proliferation of cultured cerebellar granule cells Dev. Brain Res. 111 1998 177 188
29. S.C. Danzer, E. Pan, S. Nef, L.F. Parada, and J.O. McNamara Altered regulation of brain-derived neurotrophic factor protein in hippocampus following slice preparation Neuroscience 126 2004 859 869
30. C.P. Davey Physical exertion and mental performance Ergonomics 16 1973 595 599
31. D.M.W. De Coverly Veale Exercise and mental health Acta Psychiatr. Scand. 76 1987 113 120
32. R.K. Dishman Medical psychology in exercise and sports Med. Clin. North Am. 69 1985 123 143
33. C. Dolci, A. Montaruli, E. Roveda, I. Barajon, L. Vizzotto, G.G. Zucconi, and F. Carandente Circadian variations in expression of the trkB receptor in adult rat hippocampus Brain Res. 994 2003 67 72
34. C. D'Sa, and R.S. Duman Antidepressants and neuroplasticity Bipolar Disord. 4 2002 183 194
35. R.S. Duman, G.R. Heninger, and E.J. Nestler A molecular and cellular theory of depression Arch. Gen. Psychiatry 54 1997 597 606
36. R.S. Duman, J. Malberg, S. Nakagawa, and C. D'Sa Neuronal plasticity and survival in mood disorders Biol. Psychiatry 48 2000 732 739
37. 3H]-idazoxan binding sites Br. J. Pharmacol. 118 1996 2029 2036
38. X. Fang, S.X. Yu, Y. Lu, R.C. Bast, J.R. Woodgett, and G.B. Mills Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A Proc. Natl. Acad. Sci. U. S. A. 97 2000 11960 11965
39. J.P. Fawcett, S.X. Bamji, C.G. Causing, R. Aloyz, A.R. Ase, T.A. Reader, J.H. McLean, and F.D. Miller Functional evidence that BDNF is an anterograde neurotrophic factor in the CNS J. Neurosci. 18 1998 2808 2821
40. N. Filippa, C.L. Sable, C. Filloux, B. Hemmings, and E. van Obberghen Mechanism of protein kinase B activation by cyclic AMP-dependent protein kinase Mol. Cell. Biol. 19 1999 4989 5000
41. S. Finkbeiner, S.F. Tavazoie, A. Maloratsky, K.M. Jacobs, K.M. Harris, and M.E. Greenberg CREB: a major mediator of neurotrophin responses Neuron 19 1997 1031 1047
42. D.E. Fordyce, and J.M. Wehner Physical activity enhances spatial learning performance with an associated alteration in hippocampal protein kinase c activity in C57BL/6 and DBA/2 mice Brain Res. 619 1993 111 119
43. L. Frank, R. Ventimiglia, K. Anderson, R.M. Lindsay, and J.S. Rudge BDNF down-regulates neurotrophin responsiveness, trkB protein and trkB mRNA levels in cultured rat hippocampal neurons Eur. J. Neurosci. 8 1996 1220 1230
44. T.F. Franke, D.R. Kaplan, and L.C. Cantley PI3K: downstream AKTion blocks apoptosis Cell 88 1997 435 437
45. K. Fujimaki, S. Morinobu, and R.S. Duman Administration of a cAMP phosphodiesterase 4 inhibitor enhances antidepressant-induction of BDNF mRNA in rat hippocampus Neuropsychopharmacology 22 2000 42 51
46. J.A. Garcia-Sevilla, P.V. Escribá, M. Sastre, C. Walzer, X. Busquets, G. Jaquet, D.J. Reis, and J. Guimón Immunodetection and quantitation of imidazoline receptor proteins in platelets of patients with major depression and in brains of suicide victims Arch. Gen. Psychiatry 53 1996 803 810
47. A.A. Garza, T.G. Ha, C. Garcia, M.J. Chen, and A.A. Russo-Neustadt Exercise, antidepressant treatment, and BDNF mRNA expression in the aging brain Pharmacol. Biochem. Behav. 77 2004 209 220
48. F. Gomez-Pinnila, Z. Ying, R.R. Roy, R. Molteni, and V.R. Edgerton Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity J. Neurophysiol. 88 2002 2187 2195
49. E. Gould, P. Tanapat, T. Rydel, and N. Hastings Regulation of hippocampal neurogenesis in adulthood Biol. Psychiatry 48 2000 715 720
50. H.M. Heerssen, and R.A. Segal Location, location, location: a spatial view of neurotrophin signal transduction Trends Neurosci. 25 2002 160 165
51. M. Hetman, K. Kanning, J.E. Cavanaugh, and Z. Xia Neuroprotection by brain-derived neurotrophic factor is mediated by extracellular signal-regulated kinase and phosphatidylinositol 3-kinase J. Biol. Chem. 274 1999 22569 22580
52. M. Hetman, J.E. Cavanaugh, D. Kimelman, and Z. Xia Role of glycogen synthase kinase-3β in neuronal apoptosis induced by trophic withdrawal J. Neurosci. 20 2000 2567 2574
53. R.D. Hill, M. Storandt, and M. Malley The impact of long-term exercise training on psychological function in older adults J. Gerontol., Psychol. Sci. 48 1993 P12 P17
54. K. Hisaoka, A. Nishida, T. Koda, M. Miyata, H. Zensho, S. Morinobu, M. Ohta, and S. Yamawaki Antidepressant drug treatment induce glial cell line-derived neurotrophic factor (GDNF) synthesis and release from rat C6 glioblastoma cells J. Neurochem. 79 2001 25 34
55. D. Hörsch, and C.R. Kahn Region-specific mRNA expression of phosphatidylinositol 3-kinase regulatory isoforms in the central nervous system of C57BL/6J mice J. Comp. Neurol. 415 1999 105 120
56. E.J. Huang, and L.F. Reichardt Trk receptors: roles in neuronal signal transduction Annu. Rev. Biochem. 72 2003 609 642
57. T. Hunter Signaling-2000 and beyond Cell 100 2000 113 127
58. K. Imahori, and T. Uchida Physiology and pathology of tau protein kinases in relation to Alzheimer's disease J. Biochem. 121 1997 179 188
59. A.H. Ismail, and A.M. El Naggar Effect of exercise on cognitive processing in adult men J. Hum. Ergol. 10 1981 83 91
60. A.S. Ivy, F.G. Rodrigues, C. Garcia, M.J. Chen, and A.A. Russo-Neustadt Noradrenergic and serotonergic blockade inhibits BDNF mRNA activation following exercise and antidepressant Pharmacol. Biochem. Behav. 75 2003 81 88
61. B.L. Jacobs, H. Van Praag, and F.H. Gage Adult brain neurogenesis and psychiatry: a novel theory of depression Mol. Psychiatry 5 2000 262 269
62. K.L. Jin, X.O. Mao, T. Nagayama, P.C. Goldsmith, and D.A. Greenberg Induction of vascular endothelial growth factor receptors and phosphatidylinositol 3′-kinase/Akt signaling by global cerebral ischemia in the rat Neuroscience 100 2000 713 717
63. J.D. Jordan, E.M. Landau, and R. Iyengar Signaling networks: the origins of cellular multitasking Cell 103 2000 193 200
64. K. Kitagawa, K. Takasawa, K. Kuwabara, T. Sasaki, S. Tanaka, T. Mabuchi, S. Sugiura, E. Omura-Matsuoka, M. Matsumoto, and M. Hori Differential Akt phosphorylation at ser473 and thr308 in cultured neurons after exposure to glutamate in rats Neurosci. Lett. 333 2002 187 190
65. S. Kumari, X. Liu, T. Nguyen, X. Zhang, and S.R. D'Mello Distinct phosphorylation patterns underlie Akt activation by different survival factors in neurons Brain Res., Mol. Brain Res. 96 2001 157 162
66. E.E. Labbé, M.C. Welsh, and D. Delaney Effects of consistent aerobic exercise on the psychological functioning of women Percept. Mot. Skills 67 1988 919 925
67. J.R. Lacour, J. Fourcade, L. Peyrin, and G. Vigneaud Influence de l'exercise submaximal prolongé sur les performances mentales Sci. Mot. 4 1988 188 192
68. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 277 1970 680 685
69. J.J. Lanzillo, F.-S. Yu, J. Stevens, and P.M. Hassoun Determination of xanthine dehydrogenase mRNA by a reverse transcription-coupled competitive quantitative polymerase chain reaction assay: regulation in rat endothelial cells by hypoxia and hyperoxia Arch. Biochem. Biophys. 335 1996 377 380
70. R. Lee, P. Kermani, K.K. Teng, and B.L. Hempstead Regulation of cell survival by secreted proneurotrophins Science 294 2001 1945 1948
71. T.H. Lee, H. Kato, S.T. Chen, K. Kogure, and Y. Itoyama Expression disparity of brain-derived neurotrophic factor immunoreactivity and mRNA in ischemic hippocampal neurons NeuroReport 13 2002 2271 2275
72. K. Leroy, and J.-P. Brion Developmental expression and localization of glycogen synthase kinase-3β in rat brain J. Chem. Neuroanat. 16 1999 279 293
73. M. Li, X. Wang, M.K. Meintzer, T. Laessig, M.J. Birnbaum, and K.A. Heidenreich Cyclic AMP promotes neuronal survival by phosphorylation of glycogen synthase kinase 3β Mol. Cell. Biol. 20 2000 9356 9363
74. O.H. Lowry, N.J. Rosenbrough, L.A. Farr, and R.J. Randaller Protein measurement with the folin phenol reagent J. Biol. Chem. 193 1951 265 275
75. H. Manev, T. Uz, N.R. Smalheiser, and R. Manev Antidepressants alter cell proliferation in the adult brain in vivo and in neural cultures in vitro Eur. J. Pharmacol. 411 2001 67 70
76. trkB in primary hippocampal pyramidal cell culture J. Neurosci. 13 1993 4281 4292
77. T. Matsumoto, T. Numakawa, N. Adachi, D. Yokomaku, S. Yamagishi, N. Takei, and H. Hatanaka Brain-derived neurotrophic factor enhances depolarization-evoked glutamate release in cultured cortical neurons J. Neurochem. 79 2001 522 530
78. B.S. McEwen Stress and hippocampal plasticity Annu. Rev. Neurosci. 22 1999 105 122
79. B.S. McEwen Effects of adverse experiences for brain structure and function Biol. Psychiatry 48 2000 721 731
80. L. Minichiello, F. Casagranda, R.S. Tatche, C.L. Stucky, A. Postigo, G.R. Lewin, A.M. Davies, and R. Klein Point mutation in trkB causes loss of NT-4-dependent neurons without major effects on diverse BDNF responses Neuron 21 1998 335 345
81. R. Molteni, R.J. Barnard, Z. Ying, C.K. Roberts, and F. Gómez-Pinilla A high-fat, refined sugar diet reduces hippocampal brain-derived neurotrophic factor, neuronal plasticity, and learning Neuroscience 112 2002 803 814
82. R. Molteni, Z. Ying, and F. Gómez-Pinilla Differential effects of acute and chronic exercise on plasticity-related genes in the rat hippocampus revealed by microarray Eur. J. Neurosci. 16 2002 1107 1116
83. W.P. Morgan Affective beneficence of vigorous physical activity Med. Sci. Sports Exercise 17 1985 94 100
84. S. Morinobu, K. Fujimaki, N. Okuyama, M. Takahashi, and R.S. Duman Stimulation of adenylyl cyclase and induction of brain-derived neurotrophic factor and TrkB mRNA by NKH477, a novel and potent forskolin derivative J. Neurochem. 72 1999 2198 2205
85. J. Nakae, B.-C. Park, and D. Accili Insulin stimulates phosphorylation of the forkhead transcription factor FKHR on serine 253 through a wortmannin-sensitive pathway J. Biol. Chem. 274 1999 15982 15985
86. J. Nakae, V. Barr, and D. Accili Differential regulation of gene expression by insulin and IGF-1 receptors correlates with phosphorylation of a single amino acid residue in the forkhead transcription factor FKHR EMBO J. 19 2000 989 996
87. S. Nakagawa, J.-E. Kim, R. Lee, J. Malberg, J. Chen, C. Steffan, Y.-J. Zhang, E.J. Nestler, and R.S. Duman Regulation of neurogenesis in adult mouse hippocampus by cAMP and the cAMP response element-binding protein J. Neurosci. 22 2002 3673 3682
88. N. Nakamura, S. Ramaswamy, F. Vazquez, S. Signoretti, M. Loda, and W.R. Sellers Forkhead transcription factors are critical effectors of cell death and cell cycle arrest downstream of PTEN Mol. Cell. Biol. 20 2000 8969 8982
89. A.J. Nazarali, G.B. Baker, R.T. Coutts, and T.F.J. Wong N-(2-Cyanoethyl)tranylcypromine, a potential prodrug of tranylcypromine: its disposition and interaction with catecholamine neurotransmitters in brain Pharm. Res. 4 1987 16 20
90. S.A. Neeper, F. Gómez-Pinilla, J. Choi, and C.W. Cotman Exercise and brain neurotrophins Nature 373 1995 109
91. S.A. Neeper, F. Gómez-Pinilla, J. Choi, and C.W. Cotman Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain Brain Res. 726 1996 49 56
92. M. Nibuya, S. Morinobu, and R.S. Duman Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatment J. Neurosci. 15 1995 7539 7547
93. M. Nibuya, E.J. Nestler, and R.S. Duman Chronic antidepressant administration increases the expression of cAMP response element binding protein (CREB) in rat hippocampus J. Neurosci. 16 1996 2365 2372
94. S. Noselli, and N. Perrimon Are there close encounters between signaling pathways? Science 290 2000 68 69
95. N. Noshita, A. Lewén, T. Sugawara, and P.H. Chen Akt phosphorylation and neuronal survival after traumatic brain injury in mice Neurobiol. Dis. 9 2002 294 304
96. A. Obermeier, R. Lammers, K.H. Wiesmuller, G. Jung, J. Schlessinger, and A. Ullrich Identification of trk binding sites for SHC and phosphatidylinositol 3′-kinase and formation of a multimeric signaling complex J. Biol. Chem. 268 1993 22963 22966
97. H.S. Oliff, N.C. Berchtold, P. Isackson, and C.W. Cotman Exercise-induced regulation of brain-derived neurotrophic factor (BDNF) transcripts in the rat hippocampus Mol. Brain Res. 61 1998 147 153
98. Y.B. Ouyang, X.H. Zhang, Q.P. He, G.X. Wang, B.K. Siesjo, and B.R. Hu Differential phosphorylation at ser473 and thr308 of Akt-1 in rat brain following hypoglycemic coma Brain Res. 876 2000 191 195
99. A. Patapoutian, and L.F. Reichardt Trk receptors: mediators of neurotrophin action Curr. Opin. Neurobiol. 11 2001 272 280
100. J.-J. Pei, T. Tanaka, Y.-C. Tung, E. Braak, K. Iqbal, and I. Grundke-Iqbal Distribution, levels, and activity of glycogen synthase kinase-3 in the Alzheimer disease brain J. Neuropathol. Exp. Neurol. 56 1997 70 78
101. J.-J. Pei, E. Braak, H. Braak, I. Grundke-Iqbal, K. Iqbal, B. Winblad, and R.F. Cowburn Distribution of active glycogen synthase kinase 3β (GSK-3β) in brains staged for Alzheimer disease neurofibrillary changes J. Neuropathol. Exp. Neurol. 58 1999 1010 1019
102. T. Pizzorusso, G.M. Ratto, E. Putignano, and L. Maffei Brain-derived neurotrophic factor causes cAMP response element binding protein phosphorylation in absence of calcium increases in slices and cultured neurons from rat visual cortex J. Neurosci. 20 2000 2809 2816
103. A. Pokorska, P. Vanhoutte, F.J.L. Arnold, F. Silvagno, G.E. Hardingham, and H. Bading Synaptic activity induces signaling to CREB without increasing global levels of cAMP in hippocampal neurons J. Neurochem. 84 2003 447 452
104. M. Popoli, N. Brunello, J. Perez, and G. Racagni Second messenger-regulated protein kinases in the brain: their functional role and the action of antidepressant drugs J. Neurochem. 74 2000 21 33
105. Z. Radák, T. Kaneko, S. Tahara, H. Nakamoto, J. Pucsok, M. Sasvári, C. Nyakas, and S. Goto Regular exercise improves cognitive function and decreases oxidative damage in rat brain Neurochem. Int. 38 2001 17 23
106. J.S. Raglin, and W.P. Morgan Influence of exercise and quiet rest on state anxiety and blood pressure Med. Sci. Sports Exercise 19 1987 456 463
107. G. Rena, S. Guo, S.C. Cichy, T.G. Unterman, and P. Cohen Phosphorylation of the transcription factor forkhead family member FKHR by protein kinase B J. Biol. Chem. 274 1999 17179 17183
108. E.E. Rodgers, and A.B. Theibert Functions of PI 3-kinase in development of the nervous system Int. J. Dev. Neurosci. 20 2002 187 197
109. C. Rommel, B.A. Clarke, S. Zimmermann, L. Nunez, R. Rossman, K. Reid, K. Moelling, G.D. Yancopoulos, and D.J. Glass Differentiation stage-specific inhibition of the Raf-MEK-ERK pathway by Akt Science 286 1999 1738 1741
110. A. Russo-Neustadt, R.C. Beard, and C.W. Cotman Exercise, antidepressant medications, and enhanced brain derived neurotrophic factor expression Neuropsychopharmacology 21 1999 679 682
111. A.A. Russo-Neustadt, R.C. Beard, Y.M. Huang, and C.W. Cotman Physical activity and antidepressant treatment potentiate the expression of specific brain-derived neurotrophic factor transcripts in the rat hippocampus Neuroscience 101 2000 305 312
112. A. Russo-Neustadt, T. Ha, R. Ramirez, and J.P. Kesslak Physical activity-antidepressant treatment combination: impact on brain-derived neurotrophic factor and behavior in an animal model Behav. Brain Res. 120 2001 87 95
113. T. Saarelainen, P. Hendolin, G. Lucas, E. Koponen, M. Sairanen, E. MacDonald, K. Agerman, A. Haapasalo, H. Nawa, R. Aloyz, P. Ernfors, and E. Castrén Activation of the trkB neurotrophin receptor is induced by antidepressant drugs and is required for antidepressant-induced behavioral effects J. Neurosci. 23 2003 349 357
114. R.M. Sapolsky The possibility of neurotoxicity in the hippocampus in major depression: a primer on neuron death Biol. Psychiatry 48 2000 755 765
115. R.A. Segal Selectivity in neurotrophin signaling: theme and variations Annu. Rev. Neurosci. 26 2003 299 330
116. R.A. Segal, and M.E. Greenberg Intracellular signaling pathways activated by neurotrophic factors Annu. Rev. Neurosci. 19 1996 463 489
117. A.J. Shaywitz, and M.E. Greenberg CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals Annu. Rev. Biochem. 68 1999 821 861
118. R.C. Shelton Cellular mechanisms in the vulnerability to depression and response to antidepressants Psychiatr. Clin. North Am. 23 2000 713 729
119. H. Shen, L. Tong, R. Balazs, and C.W. Cotman Physical activity elicits sustained activation of the cyclic AMP response element-binding protein and mitogen-activated protein kinase in the rat hippocampus Neuroscience 107 2001 219 239
120. P.B. Shieh, and A. Ghosh Molecular mechanisms underlying activity-dependent regulation of BDNF expression J. Neurobiol. 41 1999 127 134
121. Y. Shirayama, A.C.-H. Chen, S. Nakagawa, D.S. Russell, and R.S. Duman Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression J. Neurosci. 22 2002 3251 3261
122. J.A. Siuciak, D.R. Lewis, S.J. Wiegand, and R.M. Lindsay Antidepressant-like effect of brain-derived neurotrophic factor (BDNF) Pharmacol. Biochem. Behav. 56 1997 131 137
123. S.D. Skaper, and F.S. Walsh Neurotrophic molecules: strategies for designing effective therapeutic molecules in neurodegeneration Mol. Cell. Neurosci. 12 1998 179 193
124. V. Soontornniyomkij, G. Wang, C.A. Pittman, R.L. Hamilton, C.A. Wiley, and C.L. Achim Absence of brain-derived neurotrophic factor and trkB receptor immunoreactivity in glia of Alzheimer's disease Acta Neuropathol. 98 1999 345 348
125. A.K. Srivastava, and S.K. Pandey Potential mechanism(s) involved in the regulation of glycogen synthesis by insulin Mol. Cell. Biochem. 182 1998 135 141
126. T. Suzuki, P.J. Higgins, and D.R. Crawford Control selection for RNA quantitation BioTechniques 29 2000 332 337
127. M. Takahashi, K. Tomizawa, and K. Ishiguro Distribution of tau protein kinase I/glycogen synthase kinase-3β, phosphatases 2A and 2B, and phosphorylated tau in the developing rat brain Brain Res. 857 2000 193 206
128. J. Thome, N. Sakai, K.-H. Shin, C. Steffen, Y.-J. Zhang, S. Imprey, D. Storm, and R.S. Duman cAMP response element-mediated gene transcription is upregulated by chronic antidepressant treatment J. Neurosci. 20 2000 4030 4036
129. L. Tong, H. Shen, V.M. Perreau, R. Balazs, and C.W. Cotman Effects of exercise on gene expression profile in the rat hippocampus Neurobiol. Dis. 8 2001 1046 1056
130. 2A receptor-mediated regulation of brain-derived neurotrophic factor mRNA in the hippocampus and neocortex J. Neurosci. 17 1997 2785 2795
131. A.R. Vaillant, I. Mazzoni, C. Tudan, M. Boudreau, D.R. Kaplan, and F.D. Miller Depolarization and neurotrophins converge on the phosphatidylinositol 3-kinase-Akt pathway to synergistically regulate neuronal survival J. Cell Biol. 146 1999 955 966
132. H. Van Praag, G. Kempermann, and F.H. Gage Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus Nat. Neurosci. 2 1999 266 270
133. H. Van Praag, G. Kempermann, and F.H. Gage Neural consequences of environmental enrichment Nat. Rev. 1 2000 191 198
134. S. Vaynman, Z. Ying, and F. Gomez-Pinilla Interplay between brain-derived neurotrophic factor and signal transduction modulators in the regulation of the effects of exercise on synaptic plasticity Neuroscience 122 2003 647 657
135. S.J. Wang, N. Omori, F. Li, W.R. Zhang, G. Jin, Y. Hamakawa, K. Sato, I. Nagano, M. Shoji, and K. Abe Enhanced expression of phospho-Akt by electro-acupuncture in normal rat brain Neurol. Res. 24 2002 719 724
136. J. Widenfalk, L. Olson, and P. Thorén Deprived of habitual running, rats downregulate BDNF and TrkB messages in the brain Neurosci. Res. 34 1999 125 132
137. F. Zafra, D. Lindholm, E. Castren, J. Hartikka, and H. Thoenen Regulation of brain-derived neurotrophic factor and nerve growth factor mRNA in primary cultures of hippocampal neurons and astrocytes J. Neurosci. 12 1992 4793 4799