Molecular aspects involved in swimming exercise training reducing anhedonia in a rat model of depression

Neuroscience

Volumn 192, Issue , 2011, Pages 661-674

  Sigwalt, A R ^a   Budde, H ^b,e   Helmich, I ^c   Glaser, V ^a   Ghisoni, K ^a   Lanza, S ^a   Cadore, E L ^d   Lhullier, F L R ^d   de Bem, A F ^a   Hohl, A ^a   de Matos, F J ^a   de Oliveira, P A ^a   Prediger, R D ^a   Guglielmo, L G A ^a   Latini, A ^a  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^b HUMBOLDT UNIVERSITY   (Germany)

^c GERMAN SPORT UNIVERSITY COLOGNE   (Germany)

^d FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^e Suwon University   (South Korea)

Author keywords

Dexamethasone; Exercise training; Increased IL 10; Sucrose preference test; Testosterone; Total BDNF

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CHOLESTEROL; CORTICOSTERONE; DNA; FLUOXETINE; INTERLEUKIN 10; SUCROSE; TESTOSTERONE;

ADRENAL DISEASE; AEROBIC EXERCISE; ANHEDONIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY MASS; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; DISEASE SEVERITY; DNA METABOLISM; GLUCOSE INTAKE; HIPPOCAMPUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION; MALE; MOLECULAR BIOLOGY; NONHUMAN; ORGAN WEIGHT; PRIORITY JOURNAL; RAT; SWIMMING; TESTOSTERONE BLOOD LEVEL; TREATMENT DURATION; TREATMENT RESPONSE; WEIGHT REDUCTION;

ANHEDONIA; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; DEPRESSION; DEXAMETHASONE; DISEASE MODELS, ANIMAL; GENE EXPRESSION; GLUCOCORTICOIDS; HIPPOCAMPUS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INTERLEUKIN-10; MALE; PHYSICAL CONDITIONING, ANIMAL; PITUITARY-ADRENAL SYSTEM; RATS; RATS, WISTAR; REAL-TIME POLYMERASE CHAIN REACTION; SWIMMING;

EID: 80052265982     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.05.075     Document Type: Article

References (105)

1. Febbraio M.A., Pedersen B.K. Muscle-derived interleukin-6: mechanisms for activation and possible biological roles. FASEB J 2002, 16:1335-1347.
2. Aguiar A.S., Speck A.E., Prediger R.D., Kapczinski F., Pinho R.A. Downhill training upregulates mice hippocampal and striatal brain-derived neurotrophic factor levels. J Neural Transm 2008, 115:1251-1255.
3. Aguiar A.S., Tuon T., Pinho C.A., Silva L.A., Andreazza A.C., Kapczinski F., Quevedo J., Streck E.L., Pinho R.A. Mitochondrial IV complex and brain neurothrophic derived factor responses of mice brain cortex after downhill training. Neurosci Lett 2007, 426:171-174.
4. Diagnostic and statistical manual of mental disorders 2000, American Psychiatric Association, APA Press, Washington, DC. 4th ed.
5. Azcoitia I., Sierra A., Veiga S., Honda S., Harada N., Garcia-Segura L.M. Brain aromatase is neuroprotective. J Neurobiol 2001, 47:318-329.
6. Barden N. Implication of the hypothalamic-pituitary-adrenal axis in the physiopathology of depression. J Psychiatry Neurosci 2004, 29:185-193.
7. Beneke R. Methodological aspects of maximal lactate steady state-implications for performance testing. Eur J Appl Physiol 2003, 89:95-99.
8. Berton O., Nestler E.J. New approaches to antidepressant drug discovery: beyond monoamines. Nat Rev Neurosci 2006, 7:137-151.
9. Bi R., Broutman G., Foy M.R., Thompson R.F., Baudry M. The tyrosine kinase and mitogen-activated protein kinase pathways mediate multiple effects of estrogen in hippocampus. Proc Natl Acad Sci U S A 2000, 97:3602-3607.
10. Białek M., Zaremba P., Borowicz K.K., Czuczwar S.J. Neuroprotective role of testosterone in the nervous system. Pol J Pharmacol 2004, 56:509-518.
11. Blumenthal J.A., Babyak M.A., Moore K.A., Craighead W.E., Herman S., Khatri P., Waugh R., Napolitano M.A., Forman L.M., Appelbaum M., Doraiswamy P.M., Krishnan K.R. Effects of exercise training on older patients with major depression. Arch Intern Med 1999, 159:2349-2356.
12. Bremner J.D., Narayan M., Anderson E.R., Staib L.H., Miller H.L., Charney D.S. Hippocampal volume reduction in major depression. Am J Psychiatry 2000, 157:115-118.
13. Budde H., Pietrassyk-Kendziorra S., Bohm S., Voelcker-Rehage C. Hormonal responses to physical and cognitive stress in a school setting. Neurosci Lett 2010, 474:131-134.
14. Budde H., Voelcker-Rehage C., Pietrassyk-Kendziorra S., Machado S., Ribeiro P., Arafat A.M. Steroid hormones in the saliva of adolescents after different exercise intensities and their influence on working memory in a school setting. Psychoneuroendocrinology 2010, 35:382-391.
15. Cadore E.L., Pinto R.S., Lhullier F.L., Correa C.S., Alberton C.L., Pinto S.S., Almeida A.P., Tartaruga M.P., Silva E.M., Kruel L.F. Physiological effects of concurrent training in elderly men. Int J Sports Med 2010, 31:689-697.
16. Casarotto P.C., Andreatini R. Repeated paroxetine treatment reverses anhedonia induced in rats by chronic mild stress or dexamethasone. Eur Neuropsychopharmacol 2007, 17:735-742.
17. Cassano P., Fava M. Depression and public health: an overview. J Psychosom Res 2002, 53:849-857.
18. Castrén E. Is mood chemistry?. Nat Rev Neurosci 2005, 6:241-246.
19. Chapman D.P., Perry G.S. Depression as a major component of public health for older adults. Prev Chronic Dis 2008, 5:A22.
20. Cherrier M.M., Matsumoto A.M., Amory J.K., Asthana S., Bremner W., Peskind E.R., Raskind M.A., Craft S. Testosterone improves spatial memory in men with Alzheimer disease and mild cognitive impairment. Neurology 2005, 64:2063-2068.
21. Craft L.L., Landers D.M. The effect of exercise on clinical depression and depression resulting from mental illness: a meta-analysis. J Sport Exerc Psychol 1998, 20:339-357.
22. Day J.R., Frank A.T., O'Callaghan J.P., Jones B.C., Anderson J.E. The effect of age and testosterone on the expression of glial fibrillary acidic protein in the rat cerebellum. Exp Neurol 1998, 151:343-346.
23. Dechant G., Barde Y.A. The neurotrophin receptor p75(NTR): novel functions and implications for diseases of the nervous system. Nat Neurosci 2002, 5:1131-1136.
24. Dougherty K.D., Milner T.A. p75NTR immunoreactivity in the rat dentate gyrus is mostly within presynaptic profiles but is also found in some astrocytic and postsynaptic profiles. J Comp Neurol 1999, 407:77-91.
25. Duman R.S. Neurotrophic factors and regulation of mood: role of exercise, diet and metabolism. Neurobiol Aging 2005, 26(Suppl 1):88-93.
26. Duman R.S., Monteggia L.M. A neurotrophic model for stress-related mood disorders. Biol Psychiatry 2006, 59:1116-1127.
27. Ehninger D., Kempermann G. Regional effects of wheel running and environmental enrichment on cell genesis and microglia proliferation in the adult murine neocortex. Cereb Cortex 2003, 13:845-851.
28. Fabel K., Tam B., Kaufer D., Baiker A., Simmons N., Kuo C.J., Palmer T.D. VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci 2003, 18:2803-2812.
29. Fava M., Davidson K.G. Definition and epidemiology of treatment-resistant depression. Psychiatr Clin North Am 1996, 19:179-200.
30. Feng Y., Rhodes P.G., Liu H., Bhatt A.J. Dexamethasone induces neurodegeneration but also up-regulates vascular endothelial growth factor A in neonatal rat brains. Neuroscience 2009, 158:823-832.
31. Frazer C.J., Christensen H., Griffiths K.M. Effectiveness of treatments for depression in older people. Med J Aust 2005, 182:627-632.
32. Frye C.A., Reed T.A. Androgenic neurosteroids: anti-seizure effects in an animal model of epilepsy. Psychoneuroendocrinology 1998, 23:385-399.
33. Garcia-Garcia A.L., Elizalde N., Matrov D., Harro J., Wojcik S.M., Venzala E., Ramírez M.J., Del Rio J., Tordera R.M. Increased vulnerability to depressive-like behavior of mice with decreased expression of VGLUT1. Biol Psychiatry 2009, 66:275-282.
34. Giltay E.J., Tishova Y.A., Mskhalaya G.J., Gooren L.J., Saad F., Kalinchenko S.Y. Effects of testosterone supplementation on depressive symptoms and sexual dysfunction in hypogonadal men with the metabolic syndrome. J Sex Med 2010, 7:2572-2582.
35. Gobatto C.A., de Mello M.A., Sibuya C.Y., de Azevedo J.R., dos Santos L.A., Kokubun E. Maximal lactate steady state in rats submitted to swimming exercise. Comp Biochem Physiol A Mol Integr Physiol 2001, 130:21-27.
36. Gold S.M., Voskuhl R.R. Testosterone replacement therapy for the treatment of neurological and neuropsychiatric disorders. Curr Opin Investig Drugs 2006, 7:625-630.
37. Gomes R.J., de Oliveira C.A., Ribeiro C., Mota C.S., Moura L.P., Tognoli L.M., Leme J.A., Luciano E., de Mello M.A. Effects of exercise training on hippocampus concentrations of insulin and IGF-1 in diabetic rats. Hippocampus 2009, 19:981-987.
38. Gourley S.L., Wu F.J., Kiraly D.D., Ploski J.E., Kedves A.T., Duman R.S., Taylor J.R. Regionally specific regulation of ERK MAP kinase in a model of antidepressant-sensitive chronic depression. Biol Psychiatry 2008, 63:353-359.
39. Grandys M., Majerczak J., Duda K., Zapart-Bukowska J., Kulpa J., Zoladz J.A. Endurance training of moderate intensity increases testosterone concentration in young, healthy men. Int J Sports Med 2009, 30:489-495.
40. Greenwood B.N., Foley T.E., Day H.E., Campisi J., Hammack S.H., Campeau S., Maier S.F., Fleshner M. Freewheel running prevents learned helplessness/behavioral depression: role of dorsal raphe serotonergic neurons. J Neurosci 2003, 23:2889-2898.
41. Hansen A.H., Nielsen J.J., Saltin B., Hellsten Y. Exercise training normalizes skeletal muscle vascular endothelial growth factor levels in patients with essential hypertension. J Hypertens 2010, 28:1176-1185.
42. Hayes V.Y., Towner M.D., Isackson P.J. Organization, sequence and functional analysis of a mouse BDNF promoter. Brain Res Mol Brain Res 1997, 45:189-198.
43. Helmich I., Latini A., Sigwalt A., Carta M., Machado S., Velasques B., Ribeiro P., Budde H. Neurobiological alterations induced by exercise and their impact on depressive disorders. Clinical Practice & Epidemiology in mental health 6 2000.
44. Hintikka J., Niskanen L., Koivumaa-Honkanen H., Tolmunen T., Honkalampi K., Lehto S.M., Viinamäki H. Hypogonadism, decreased sexual desire, and long-term depression in middle-aged men. J Sex Med 2009, 6:2049-2057.
45. Hoffman B.M., Babyak M.A., Craighead W.E., Sherwood A., Doraiswamy P.M., Coons M.J., Blumenthal J.A. Exercise and pharmacotherapy in patients with major depression: one-year follow-up of the SMILE study. Psychosom Med 2011, 73:127-133.
46. Holsboer F. The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology 2000, 23:477-501.
47. Hu Y., Asano K., Mizuno K., Usuki S., Kawakura Y. Serum testosterone responses to continuous and intermittent exercise training in male rats. Int J Sports Med 1999, 20:12-16.
48. Kahn S.E., Hull R.L., Utzschneider K.M. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 2006, 444:840-846.
49. Kaiserman I., Avni M., Sack J. Kinetics of the pituitary-thyroid axis and the peripheral thyroid hormones in 2 children with thyroxine intoxication. Horm Res 1995, 44:229-237.
50. Katoh-Semba R., Takeuchi I.K., Semba R., Kato K. Distribution of brain-derived neurotrophic factor in rats and its changes with development in the brain. J Neurochem 1997, 69:34-42.
51. Kernie S.G., Liebl D.J., Parada L.F. BDNF regulates eating behavior and locomotor activity in mice. EMBO J 2000, 19:1290-1300.
52. Koshimizu H., Kiyosue K., Hara T., Hazama S., Suzuki S., Uegaki K., Nagappan G., Zaitsev E., Hirokawa T., Tatsu Y., Ogura A., Lu B., Kojima M. Multiple functions of precursor BDNF to CNS neurons: negative regulation of neurite growth, spine formation and cell survival. Mol Brain 2009, 2:27.
53. Kronenberg G., Kirste I., Inta D., Chourbaji S., Heuser I., Endres M., Gass P. Reduced hippocampal neurogenesis in the GR(+/-) genetic mouse model of depression. Eur Arch Psychiatry Clin Neurosci 2009, 259:499-504.
54. Lawlor D.A., Hopker S.W. The effectiveness of exercise as an intervention in the management of depression: systematic review and meta-regression analysis of randomised controlled trials. BMJ 2001, 322:763-767.
55. Lino-de-Oliveira C., De Lima T.C., de Pádua Carobrez A. Structure of the rat behaviour in the forced swimming test. Behav Brain Res 2005, 158:242-250.
56. Marais L., Stein D.J., Daniels W.M. Exercise increases BDNF levels in the striatum and decreases depressive-like behavior in chronically stressed rats. Metab Brain Dis 2009, 24:587-597.
57. Matsakas A., Nikolaidis M.G., Kokalas N., Mougios V., Diel P. Effect of voluntary exercise on the expression of IGF-I and androgen receptor in three rat skeletal muscles and on serum IGF-I and testosterone levels. Int J Sports Med 2004, 25:502-508.
58. McCann I.L., Holmes D.S. Influence of aerobic exercise on depression. J Pers Soc Psychol 1984, 46:1142-1147.
59. McEwen B.S. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 2007, 87:873-904.
60. Militello A., Vitello G., Lunetta C., Toscano A., Maiorana G., Piccoli T., La Bella V. The serum level of free testosterone is reduced in amyotrophic lateral sclerosis. J Neurol Sci 2002, 195:67-70.
61. Moussavi S., Chatterji S., Verdes E., Tandon A., Patel V., Ustun B. Depression, chronic diseases, and decrements in health: results from the World Health Surveys. Lancet 2007, 370:851-858.
62. Mowla S.J., Pareek S., Farhadi H.F., Petrecca K., Fawcett J.P., Seidah N.G., Morris S.J., Sossin W.S., Murphy R.A. Differential sorting of nerve growth factor and brain-derived neurotrophic factor in hippocampal neurons. J Neurosci 1999, 19:2069-2080.
63. Mukai H., Tsurugizawa T., Ogiue-Ikeda M., Murakami G., Hojo Y., Ishii H., Kimoto T., Kawato S. Local neurosteroid production in the hippocampus: influence on synaptic plasticity of memory. Neuroendocrinology 2006, 84:255-263.
64. Nestler E.J., Barrot M., DiLeone R.J., Eisch A.J., Gold S.J., Monteggia L.M. Neurobiology of depression. Neuron 2002, 34:13-25.
65. Nguyen T.V., Jayaraman A., Quaglino A., Pike C.J. Androgens selectively protect against apoptosis in hippocampal neurones. J Neuroendocrinol 2010, 22:1013-1022.
66. North T.C., McCullagh P., Tran Z.V. Effect of exercise on depression. Exerc Sport Sci Rev 1990, 18:379-415.
67. Oei T.I., Verhoeven W.M., Westenberg H.G., Zwart F.M., van Ree J.M. Anhedonia, suicide ideation and dexamethasone nonsuppression in depressed patients. J Psychiatr Res 1990, 24:25-35.
68. Ono M., Ichihara J., Nonomura T., Itakura Y., Taiji M., Nakayama C., Noguchi H. Brain-derived neurotrophic factor reduces blood glucose level in obese diabetic mice but not in normal mice. Biochem Biophys Res Commun 1997, 238:633-637.
69. Pang P.T., Teng H.K., Zaitsev E., Woo N.T., Sakata K., Zhen S., Teng K.K., Yung W.H., Hempstead B.L., Lu B. Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 2004, 306:487-491.
70. Parker K.J., Schatzberg A.F., Lyons D.M. Neuroendocrine aspects of hypercortisolism in major depression. Horm Behav 2003, 43:60-66.
71. Pedersen B.K., Steensberg A., Fischer C., Keller C., Keller P., Plomgaard P., Febbraio M., Saltin B. Searching for the exercise factor: is IL-6 a candidate?. J Muscle Res Cell Motil 2003, 24:113-119.
72. Pedersen B.K., Steensberg A., Schjerling P. Muscle-derived interleukin-6: possible biological effects. J Physiol 2001, 536:329-337.
73. Phillips W.T., Kiernan M., King A.C. Physical activity as a nonpharmacological treatment for depression: a review. Complement Health Pract Rev 2003, 8:139-152.
74. Pignatelli D., Magalhães M.M., Magalhães M.C. Direct effects of stress on adrenocortical function. Horm Metab Res 1998, 30:464-474.
75. Porsolt R.D., Anton G., Blavet N., Jalfre M. Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 1978, 47:379-391.
76. Rannels S.R., Jefferson L.S. Effects of glucocorticoids on muscle protein turnover in perfused rat hemicorpus. Am J Physiol 1980, 238:E564-E572.
77. Roche M., Harkin A., Kelly J.P. Chronic fluoxetine treatment attenuates stressor-induced changes in temperature, heart rate, and neuronal activation in the olfactory bulbectomized rat. Neuropsychopharmacology 2007, 32:1312-1320.
78. Rosario E.R., Pike C.J. Androgen regulation of beta-amyloid protein and the risk of Alzheimer's disease. Brain Res Rev 2008, 57:444-453.
79. Schito M.L., Kennedy P.E., Kowal R.P., Berger E.A., Sher A. A human immunodeficiency virus-transgenic mouse model for assessing interventions that block microbial-induced proviral expression. J Infect Dis 2001, 183:1592-1600.
80. Seidah N.G., Chrétien M. Proprotein and prohormone convertases: a family of subtilases generating diverse bioactive polypeptides. Brain Res 1999, 848:45-62.
81. Seidman S.N., Rabkin J.G. Testosterone replacement therapy for hypogonadal men with SSRI-refractory depression. J Affect Disord 1998, 48:157-161.
82. Sha H., Xu J., Tang J., Ding J., Gong J., Ge X., Kong D., Gao X. Disruption of a novel regulatory locus results in decreased Bdnf expression, obesity, and type 2 diabetes in mice. Physiol Genomics 2007, 31:252-263.
83. Shores M.M., Sloan K.L., Matsumoto A.M., Moceri V.M., Felker B., Kivlahan D.R. Increased incidence of diagnosed depressive illness in hypogonadal older men. Arch Gen Psychiatry 2004, 61:162-167.
84. Stensballe J., Christiansen M., Tønnesen E., Espersen K., Lippert F.K., Rasmussen L.S. The early IL-6 and IL-10 response in trauma is correlated with injury severity and mortality. Acta Anaesthesiol Scand 2009, 53:515-521.
85. Stranahan A.M., Lee K., Mattson M.P. Central mechanisms of HPA axis regulation by voluntary exercise. Neuromol Med 2008, 10:118-127.
86. Teng H.K., Teng K.K., Lee R., Wright S., Tevar S., Almeida R.D., Kermani P., Torkin R., Chen Z.Y., Lee F.S., Kraemer R.T., Nykjaer A., Hempstead B.L. ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J Neurosci 2005, 25:5455-5463.
87. Toyokuni S., Tanaka T., Hattori Y., Nishiyama Y., Yoshida A., Uchida K., Hiai H., Ochi H., Osawa T. Quantitative immunohistochemical determination of 8-hydroxy-2'-deoxyguanosine by a monoclonal antibody N451: its application to ferric nitrilotriacetate-induced renal carcinogenesis model. Lab Invest 1997, 76:365-374.
88. Tsimberidou A.M., Estey E., Wen S., Pierce S., Kantarjian H., Albitar M., Kurzrock R. The prognostic significance of cytokine levels in newly diagnosed acute myeloid leukemia and high-risk myelodysplastic syndromes. Cancer 2008, 113:1605-1613.
89. van der Borght K., Ferrari F., Klauke K., Roman V., Havekes R., Sgoifo A., van der Zee E.A., Meerlo P. Hippocampal cell proliferation across the day: increase by running wheel activity, but no effect of sleep and wakefulness. Behav Brain Res 2006, 167:36-41.
90. van Praag H. Exercise and the brain: something to chew on. Trends Neurosci 2009, 32:283-290.
91. 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 U S A 1999, 96:13427-13431.
92. 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.
93. Vieira C., De Lima T.C., Carobrez Ade P., Lino-de-Oliveira C. Frequency of climbing behavior as a predictor of altered motor activity in rat forced swimming test. Neurosci Lett 2008, 445:170-173.
94. Weill-Engerer S., David J.P., Sazdovitch V., Liere P., Eychenne B., Pianos A., Schumacher M., Delacourte A., Baulieu E.E., Akwa Y. Neurosteroid quantification in human brain regions: comparison between Alzheimer's and nondemented patients. J Clin Endocrinol Metab 2002, 87:5138-5143.
95. Wilborn C.D., Taylor L.W., Greenwood M., Kreider R.B., Willoughby D.S. Effects of different intensities of resistance exercise on regulators of myogenesis. J Strength Cond Res 2009, 23:2179-2187.
96. Willner P. Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 2005, 52:90-110.
97. Willner P., Moreau J.L., Nielsen C.K., Papp M., Sluzewska A. Decreased hedonic responsiveness following chronic mild stress is not secondary to loss of body weight. Physiol Behav 1996, 60:129-134.
98. Wittert G.A., Livesey J.H., Espiner E.A., Donald R.A. Adaptation of the hypothalamopituitary adrenal axis to chronic exercise stress in humans. Med Sci Sports Exerc 1996, 28:1015-1019.
99. Woo N.H., Teng H.K., Siao C.J., Chiaruttini C., Pang P.T., Milner T.A., Hempstead B.L., Lu B. Activation of p75NTR by proBDNF facilitates hippocampal long-term depression. Nat Neurosci 2005, 8:1069-1077.
100. Xu B., Goulding E.H., Zang K., Cepoi D., Cone R.D., Jones K.R., Tecott L.H., Reichardt L.F. Brain-derived neurotrophic factor regulates energy balance downstream of melanocortin-4 receptor. Nat Neurosci 2003, 6:736-742.
101. Yang L.Y., Arnold A.P. Interaction of BDNF and testosterone in the regulation of adult perineal motoneurons. J Neurobiol 2000, 44:308-319.
102. Yarrow J.F., White L.J., McCoy S.C., Borst S.E. Training augments resistance exercise induced elevation of circulating brain derived neurotrophic factor (BDNF). Neurosci Lett 2010, 479:161-165.
103. Yip H.K., Youssef A.A., Chang L.T., Yang C.H., Sheu J.J., Chua S., Yeh K.H., Lee F.Y., Wu C.J., Hang C.L. Association of interleukin-10 level with increased 30-day mortality in patients with ST-segment elevation acute myocardial infarction undergoing primary coronary intervention. Circ J 2007, 71:1086-1091.
104. Zitzmann M. Testosterone and the brain. Aging Male 2006, 9:195-199.
105. Zoladz J.A., Pilc A., Majerczak J., Grandys M., Zapart-Bukowska J., Duda K. Endurance training increases plasma brain-derived neurotrophic factor concentration in young healthy men. J Physiol Pharmacol 2008, 59(Suppl 7):119-132.