High-intensity exercise training produces morphological and biochemical changes in adrenal gland of mice

Histology and Histopathology

Volumn 27, Issue 6, 2012, Pages 753-769

  Bartalucci, A ^a   Ferrucci, M ^a   Fulceri, F ^a   Lazzeri, G ^a   Lenzi, P ^a   Toti, L ^a   Serpiello, F R ^b,c   la Torre, A ^d   Gesi, M ^a  

^a UNIVERSITY OF PISA   (Italy)

^b UNIVERSITY OF VERONA   (Italy)

^c VICTORIA UNIVERSITY   (Australia)

^d UNIVERSITY OF MILAN   (Italy)

Author keywords

Adrenal gland; Electron microscopy; Morphology; Training

Indexed keywords

CATECHOLAMINE; DOPAMINE BETA MONOOXYGENASE; LACTIC ACID; PHENYLETHANOLAMINE N METHYLTRANSFERASE; TYROSINE 3 MONOOXYGENASE;

ADAPTATION; ADRENAL GLAND; ANIMAL; ARTICLE; BLOOD; C57BL MOUSE; COMPARATIVE STUDY; EXERCISE; IMMUNOHISTOCHEMISTRY; MALE; METABOLISM; MOUSE; ORGAN SIZE; PATHOLOGY; RUNNING; TIME; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; WEIGHT GAIN; WESTERN BLOTTING;

ADAPTATION, PHYSIOLOGICAL; ADRENAL GLANDS; ANIMALS; BLOTTING, WESTERN; CATECHOLAMINES; DOPAMINE BETA-HYDROXYLASE; IMMUNOHISTOCHEMISTRY; LACTIC ACID; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; ORGAN SIZE; PHENYLETHANOLAMINE N-METHYLTRANSFERASE; PHYSICAL EXERTION; RUNNING; TIME FACTORS; TYROSINE 3-MONOOXYGENASE; WEIGHT GAIN;

MUS;

EID: 84859339269     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (110)

1. Akana S.F., Shinsako J. and Dallman M.F. (1983). Relationships among adrenal weight, corticosterone, and stimulated adrenocorticotropin levels in rats. Endocrinology 113, 2226-2231.
2. Ang E.T., Tai Y.K., Lo S.Q., Seet R. and Soong T.W. (2010). Neurodegenerative diseases: exercising toward neurogenesis and neuroregeneration. Front. Aging Neurosci. 2, 1-8.
3. Angeli A., Minetto M., Dovio A. and Paccotti P. (2004). The overtraining syndrome in athletes: a stress-related disorder. J. Endocrinol. Invest. 27, 603-612.
4. Axelrod J. and Reisine T.D. (1984). Stress hormones: their interaction and regulation. Science 224, 452-459.
5. Ben Abdelkrim N., El Fazaa S. and El Ati J. (2007). Time-motion analysis and physiological data of elite under-19-year-old basketball players during competition. Br. J. Sports Med. 41, 69-75.
6. Betito K., Mitchell J.B., Bhatnagar S., Boksa P. and Meaney M.J. (1994). Regulation of the adrenomedullary catecholaminergic system after mild, acute stress. Am. J. Physiol. 267, R212-220.
7. Bilang-Bleuel A., Droste S., Gesing A., Rech J., Linthorst A.C.E and Reul J.M.H.M. (2000). Impact of stress and voluntary exercise on neurogenesis in the adult hippocampus: quantitative analysis by detection of Ki-67. Program of the 30th Annual Meeting of the Society for Neuroscience, p 1534 (Abstract).
8. Bishop D. (2001). Evaluation of the Accusport Lactate Analyzer. Int. J. Sports Med. 22, 525-530.
9. Brown D.A., Johnson M.S., Armstrong C.J., Lynch J.M., Caruso N.M., Ehlers L.B., Fleshner M., Spencer R.L. and Moore R.L. (2007). Short-term treadmill running in the rat: what kind of stressor is it? J. Appl. Physiol. 103, 1979-1985.
10. Bryant H.U., Bernton E.W., Kenner J.R. and Holaday J.W. (1991). Role of adrenal cortical activation in the immunosuppressive effects of chronic morphine treatment. Endocrinology 128, 3253-3258.
11. Buchheit M., Spencer M. and Ahmaidi S. (2010). Reliability, usefulness and validity of a repeated sprint and jump ability test. Int. J. Sports Physiol. 5, 3-17.
12. Bunt J.C. (1986). Hormonal alterations due to exercise. Sports Med. 3, 331-345.
13. Buuck R.J., Tharp G.D. and Brumbaugh J.A. (1976). Effects of chronic exercise on the ultrastructure of the adrenocortical cells in the rat. Cell Tissue Res. 168, 261-270.
14. Chen E.C. and Brzyski R.G. (1999). Exercise and reproductive dysfunction. Fertil. Steril. 71, 1-6.
15. Chrousos G.P. and Gold P.W. (1992). The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. JAMA 267, 1244-1252.
16. Coleman M.A., Garland T. Jr., Marler C.A., Newton S.S., Swallow J.G. and Carter P.A. (1998). Glucocorticoid Response to Forced Exercise in Laboratory House Mice (Mus domesticus). Physiol. Behav. 63, 279-285.
17. Colomer C., Désarmenien M.G. and Guérineau N.C. (2009). Revisiting the stimulus-secretion coupling in the adrenal medulla: role of gap junction-mediated intercellular communication. Mol. Neurobiol. 40, 87-100.
18. 2+ Channels and Adrenal Catecholamine Release by G Protein Coupled Receptors. Cell. Mol. Neurobiol. 30, 1201-1208.
19. Davies E., Omer S., Buckingham C., Morris J.F. and Christian H.C. (2007). Expression and externalization of annexin 1 in the adrenal gland: structure and function of the adrenal gland in annexin 1-null mutant mice. Endocrinology 148, 1030-1038.
20. De Boer S.F., Slangen J.L. and van der Gugten J. (1988). Adaptation of plasma catecholamine and corticosterone responses to short-term repeated noise stress in rats. Physiol. Behav. 44, 273-280.
21. Deane H.W. and Masson G.M. (1951). Adrenal cortical changes in rats with various types of experimental hypertension. J. Clin. Endocrinol. Metab. 11, 193-208.
22. Del Balso C. and Cafarelli E. (2007). Adaptations in the activation of human skeletal muscle induced by short-term isometric resistance training. J. Appl. Physiol. 103, 402-411.
23. Duclos M., Corcuff J-B., Pehourcq F. and Tabarin A. (2001). Decreased pituitary sensitivity to glucocorticoids in endurance-trained men. Eur. J. Endocrinol. 144, 363-368.
24. Dumke C.L., Rhodes J.S., Garland T. Jr., Maslowski E., Swallow J.G., Wetter A.C. and Cartee G.D. J. (2001). Genetic selection of mice for high voluntary wheel running: effect on skeletal muscle glucose uptake. J. Appl. Physiol. 91, 1289-1297.
25. Feasson L., Stockholm D., Freyssenet D., Richard I., Duguez S., Beckmann J.S. and Denis C. (2002). Molecular adaptations of neuromuscular disease-associated proteins in response to eccentric exercise in human skeletal muscle. J. Physiol. 543, 297-306.
26. Ferreira J.C.B., Rolim N.P.L., Bartholomeu J.B., Gobatto C.A., Kokubun E. and Brum P.C. (2007). Maximal lactate steady state in running mice: effect of exercise training. Clin. Exp. Pharmacol. P. 34, 760-765.
27. Fleshner M., Deak T., Spencer R.L., Laudenslager M.L., Watkins L.R. and Maier S.F. (1995). A long-term increase in basal levels of corticosterone and a decrease in corticosteroid-binding globulin after acute stressor exposure. Endocrinology 136, 5336-5342.
28. Gesi M., Fornai F., Lenzi P., Natale G., Soldani P. and Paparelli A. (2001). Time-dependent changes in adrenal cortex ultrastructure and corticosterone levels after noise exposure in male rats. Eur. J. Morphol. 39, 129-135.
29. Glaister M. (2005). Multiple sprint work. Physiological responses, mechanisms of fatigue and the influence of aerobic fitness. Sports Med. 35, 757-777.
30. Gobatto C.A., de Mello M.A., Sibuya C.Y., de Azevedo J.R., dos Santos L.A. and Kokubun E. (2001). Maximal lactate steady state in rats, submitted to swimming exercise. Comp. Biochem. Physiol. A Mol. Integr. Physiol 130, 21-7.
31. Gopinath B., Hardy L.L., Teber E. and Mitchell P. (2011). Association between physical activity and blood pressure in prepubertal children. Hypertens. Res. 34, 851-855.
32. Green H.J. (2000). Altitude acclimatization, training and performance. J. Sci. Med. Sport 3, 299-312.
33. Greep R.O. and Deane H.W. (1947). Cytochemical evidence for the cessation of hormone production in the zona glomerulosa of the rat's adrenal cortex after prolonged treatment with desoxycorticosterone acetate. Endocrinology 40, 417-425.
34. Greep R.O. and Deane H.W. (1949). The cytology and cytochemistry of the adrenal cortex. Ann. NY Acad. Sci. 50, 596-615.
35. Hagberg J.M., Park J.J. and Brown M.D. (2000). The role of exercise training in the treatment of hypertension: an update. Sports Med. 30, 193-206.
36. Halliwill J.R. (2003). Hypoxic regulation of blood flow in humans. Skeletal muscle circulation and the role of epinephrine. Adv. Exp. Med. Biol. 543, 223-236.
37. Hansen D., Dendale P., Berger J., van Loon L.J.C. and Meeusen R. (2007). The Effects of exercise training on fat-mass loss in obese patients during energy intake restriction. Sports Med. 37, 31-46.
38. Hill J.O. and Wyatt H.R. (2005). Role of physical activity in preventing and treating obesity. J. Appl. Physiol. 99, 765-770.
39. Jiang W., Uht R. and Bohn M.C. (1989). Regulation of phenylethanolamine N-methyltransferase (PNMT) mRNA in the rat adrenal medulla by corticosterone. Int. J. Dev. Neurosci. 7, 513-520.
40. Jones A.M. and Carter H. (2000). The effect of endurance training on parameters of aerobic fitness. Sports Med. 29, 373-386.
41. Joseph L.J., Prigeon R.L., Blumenthal J.B., Ryan A.S. and Goldberg A.P. (2011). Weight Loss and Low-Intensity Exercise for the Treatment of Metabolic Syndrome in Obese Postmenopausal Women. J. Gerontol. A Biol. Sci. Med. Sci. 66, 1022-1029.
42. Karsten S.L and Geschwind D.H. (2005). Exercise your amyloid. Cell 120, 572-574.
43. Katz R.J., Roth K.A. and Carroll B.J. (1981). Acute and chronic stress effects on open field activity in the rat: implications for a model of depression. Neurosci. Biobehav. Rev. 5, 247-251.
44. Kramer J.M., Plowey E.D., Beatty J.A., Little H.R. and Waldrop T.G. (2000). Hypothalamus, hypertension, and exercise. Brain Res. Bull. 53, 77-85.
45. La Monte M.J., Blair S.N. and Church T.S. (2005). Physical activity and diabetes prevention. J. Appl. Physiol. 99, 1205-1213.
46. Larson E.B., Wang L., Bowen J.D., McCormick W.C., Teri L., Crane P. and Kukull W. (2006). Exercise is associated with reduced risk for incident dementia among persons 65 years of age and older. Ann. Intern. Med. 144, 73-81.
47. Larun L., Nordheim L., Ekeland E., Hagen K. and Heian F. (2006). Exercise in prevention and treatment of anxiety and depression among children and young people. Cochrane Db. Syst. Rev. 19, CD004691.
48. Laursen P.B. (2010). Training for intense exercise performance: highintensity or high-volume training? Scand. J. Med. Sci. Sports 20, 1-10.
49. Laursen P.B. and Rhodes E.C. (2001). Factors affecting performance in an ultraendurance triathlon. Sports Med. 31, 195-209.
50. LeBrasseur N.K., Walsh K. and Arany Z. (2010). Metabolic benefits of resistance training and fast glycolytic skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 300, E3-E10.
51. Lee L.L., Watson M.C., Mulvaney C.A., Tsai C.C. and Lo S.F. (2010). The effect of walking intervention on blood pressure control: a systematic review. Int. J. Nurs. Stud. 47, 1545-1561.
52. Livezey G.T., Miller J.M. and Vogel W.H. (1985). Plasma norepinephrine, epinephrine and corticosterone stress responses to restraint in individual male and female rats, and their correlations. Neurosci. Lett. 62, 51-56.
53. Luger A., Deuster P.A., Kyle S.B., Gallucci W.T., Montgomery L.C., Gold P.W., Loriaux D.L. and Chrousos G.P. (1987). Acute hypothalamic-pituitary-adrenal response to the stress of treadmill exercise. N. Engl. J. Med. 316, 1309-1315.
54. Manchado F.B., Gobatto C.A., Contarteze R.V., Papoti M. and de Mello M.A. (2005). Maximal lactate steady state in running rats. J. Exerc. Physiol. 8, 29-35.
55. Matysiak W. and Jodłowska-Jedrych B. (2010). Does administration of non-steroidal anti-inflammatory drug determine morphological changes in adrenal cortex: ultrastructural studies. Protoplasma 246, 109-118.
56. Mazzocchi G., Malendowicz L.K., Rebuffat P., Robba C., Gottardo G. and Nussdorfer G.G. (1986). Short- and long-term effects of ACTH on the adrenal zona glomerulosa of the rat. A coupled stereological and enzymological study. Cell Tissue Res. 243, 303-310.
57. McCarty R. (1985). Sympathetic-adrenal medullary and cardiovascular responses to acute cold stress in adult and aged rats. J. Auton. Nerv. Syst. 12, 15-22.
58. Molmen-Hansen H.E., Stolen T., Tjonna A.E., Aamot I.L., Ekeberg I.S., Tyldum G.A., Wisloff U., Ingul C.B. and Stoylen A. (2011). Aerobic interval training reduces blood pressure and improves myocardial function in hypertensive patients. Eur. J. Cardiovasc. Prev. Rehabil. (in press).
59. Moraska A., Deak T., Spencer R.L., Roth D. and Fleshner M. (2000). Treadmill running produces both positive and negative physiological adaptations in Sprague-Dawley rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279, R1321-R1329.
60. Nieman D.C. (2000). Exercise effects on systemic immunity. Immunol. Cell. Biol. 78, 496-501.
61. Nussdorfer G.G. (1986). Cytophysiology of the adrenal cortex. Int. Rev. Cytol. 98, 1-405.
62. Nussdorfer G.G. and Mazzocchi G. (1982). Stereological and biochemical investigations on a possible aldosterone-containing secretory organelle in the zona glomerulosa of rat adrenal gland. Anat. Anz. 151, 74-81.
63. Nussdorfer G.G., Armato U., Mazzocchi G., Andreis P.G. and Draghi E. (1977). Investigations on turnover of adrenocortical mitochondria. IX. A stereological study of the effects of chronic treatment with ACTH on the size and number of mitochondria from adult human adrenocortical cells cultured in vitro. Cell Tissue Res. 182, 145-150.
64. Nyhuis T.J., Masini C.V., Sasse S.K., Day H.E. and Campeau S. (2010). Physical activity, but not environmental complexity, facilitates HPA axis response habituation to repeated audiogenic stress despite neurotrophin mRNA regulation in both conditions. Brain Res. 1362, 68-77.
65. Olson A.K., Eadie B.D., Ernst C. and Christie B.R. (2006). Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus 16, 250-260.
66. Opie L. (1998). Receptors and signal transduction. In: The heart: physiology, from cell to circulation. Opie L. (ed). Lippincott Williams and Wilkins. Philadelphia. pp 173-207.
67. Ottenweller J.E., Natelson B.H., Pitman D.L. and Drastal S.D. (1989). Adrenocortical and behavioral responses to repeated stressors: toward an animal model of chronic stress and stress-related mental illness. Biol. Psychiat. 26, 829-841.
68. Pagotto U., Vicennati V., Ceroni L. and Pasquali P. (2001). Lo stress e la sindrome da mal adattamento. In: Le malattie del cervello. Le Scienze - Quaderni 119, pp 66-71.
69. Pedersen B.K. and Hoffman-Goetz L. (2000). Exercise and the immune system: regulation, integration, and adaptation. Physiol. Rev. 80, 1055-1081.
70. Pellegrini A., Soldani P., Gesi M., Lenzi P., Natale G. and Paparelli A. (1997). Effect of varying noise stress duration on rat adrenal gland: An ultrastructural study. Tissue Cell 29, 597-602.
71. Perrino C., Gargiulo G., Pironti G., Franzone A., Scudiero L., De Laurentis M., Magliulo F., Ilardi F., Carotenuto G., Schiattarella G.G. and Esposito G. (2011). Cardiovascular effects of treadmill exercise in physiological and pathological preclinical settings. Am. J. Physiol. Heart Circ. Physiol. 300, H1983-H1989.
72. Peterson M.D., Sen A. and Gordon P.M. (2011). Influence of resistance exercise on lean body mass in aging adults: a meta-analysis. Med. Sci. Sports Exerc. 43, 249-258.
73. Petroviç-Oggiano G., Damjanov V., Gurinoviç M. and Glibetiç M. (2010). Physical activity in prevention and reduction of cardiovascular risk. Med. Pregl. 63, 200-207.
74. Philp A., Macdonald A.L. and Watt P.W. (2005). Lactate: a signal coordinating cell and systemic function. J. Exp. Biol. 208, 4561-4575.
75. Privalle C.T., Crivello J.F. and Jefcoate C.R. (1983). Regulation of intramitochondrial cholesterol transfer to side-chain cleavage cytochrome P-450 in rat adrenal gland. Proc. Natl. Acad. Sci. USA 80, 702-706.
76. Proske U. and Morgan D.L. (2001). Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical application. J. Physiol. 537, 333-345.
77. Purvis D., Gonsalves S. and Deuster P.A. (2010). Physiological and psychological fatigue in extreme conditions: overtraining and elite athletes. PM R. 2, 442-450.
78. Rittenhouse P.A., López-Rubalcava C., Stanwood G.D. and Lucki I. (2002). Amplified behavioral and endocrine responses to forced swim stress in the Wistar-Kyoto rat. Psychoneuroendocrinol. 27, 303-318.
79. Rothman R.B., Jayanthi S., Wang X., Dersch C.M., Cadet J.L., Prisinzano T., Rice K.C. and Baumann M.H. (2003). High-dose fenfluramine administration decreases serotonin transporter binding, but not serotonin transporter protein levels, in rat forebrain. Synapse 50, 233-239.
80. Rubin B.L., Deane H.W. and Hamilton J.A. (1963). Biochemical and histochemical studies on 3-beta-hydroxysteroid dehydrogenase activity in the adrenal glands and ovaries of diverse mammals. Endocrinology 73, 748-763.
81. Sabban E.L. and Kvetnansky R. (2001). Stress-triggered activation of gene expression in catecholaminergic systems: Dynamics of transcriptional events. Trends Neurosci. 24, 91-98.
82. Sasse S.K., Greenwood B.N., Masini C.V., Nyhuis T.J., Fleshner M., Day H.E.W. and Campeau S. (2008). Chronic voluntary wheel running facilitates corticosterone response habituation to repeated audiogenic stress exposure in male rats. Stress 11, 425-437.
83. Schulze P.C., Gielen S., Schuler G. and Hambrecht R. (2002). Chronic heart failure and skeletal muscle catabolism: effects of exercise training. Int. J. Cardiol. 85, 141-149.
84. Scomparin D.X., Grassiolli S., Marçal A.C., Gravena C., Andreazzi A.E. and Mathias P.C.F. (2006). Swim training applied at early age is critical to adrenal medulla catecholamine content and to attenuate monosodium L-glutamate-obesity onset in mice. Life Sci. 79, 2151-2156.
85. Scomparin D.X., Gomes R.M., Grassiolli S., Rinaldi W., Martins A.G., de Oliveira J.C., Gravena C. and de Freitas Mathias P.C. (2009). Autonomic activity and glycemic homeostasis are maintained by precocious and low intensity training exercises in MSG-programmed obese mice. Endocrine 36, 510-517.
86. Scribner K.A., Akana S.F., Walker C.D. and Dallman M.F. (1993). Streptozotocindiabetic rats exhibit facilitated adrenocorticotropin responses to acute stress, but normal sensitivity to feedback by corticosteroids. Endocrinology 133, 2667-2674.
87. Selye H. (1950). Stress and the general adaptation syndrome. Br. Med. J. 1, 1383-1392.
88. Shafaroudi M.M., McBride M., Deighan C., Wokoma A., Macmillan J., Daly C.J. and McGrath J.C. (2005). Two "knockout" mouse models demonstrate that aortic vasodilatation is mediated via alpha2aadrenoceptors located on the endothelium. J. Pharmacol. Exp. Ther. 314, 804-810.
89. Shephard R.J. (2005). Chronic fatigue syndrome. A brief review of functional disturbances and potential therapy. J. Sports Med. Phys. Fitness 45, 381-392.
90. Sheppard J.M., Gabbett T., Taylor K.L., Dorman J., Lebedew A.J. and Borgeaud R. (2007). Development of a repeated-effort test for elite men's volleyball. Int. J. Sports Physiol. Perform. 2, 292-304.
91. Smith S.M. and Vale W.W. (2006). The role of the hypothalamicpituitary- adrenal axis in neuroendocrine responses to stress. Dialogues Clin. Neurosci. 8, 383-395.
92. Soldani P., Gesi M., Lenzi P., Natale G., Fornai F., Pellegrini A., Ricciardi M.P. and Paparelli A. (1999). Long-term exposure to noise modifies rat adrenal cortex ultrastructure and corticosterone plasma levels. J. Submicrosc. Cytol. Pathol. 31, 441-448.
93. Spencer M., Bishop D., Dawson B. and Goodman C. (2005). Physiological and metabolic responses of repeated-sprint activities: specific to field-based team sports. Sports Med. 35, 1025-1044.
94. Stocco D.M. and Clark B.J. (1996). Role of the steroidogenic acute regulatory protein (StAR) in steroidogenesis. Biochem. Pharmacol. 51, 197-205.
95. Svedahl K. and MacIntosh B.R. (2003). Anaerobic threshold: The concept and methods of measurement. Can. J. Appl. Physiol. 28, 299-323.
96. Tabata I., Atomi Y., Kanehisa H. and Miyashita M. (1990). Effect of highintensity endurance training on isokinetic muscle power. Eur. J. Appl. Physiol. O. 60, 254-258.
97. Tai T.C., Claycomb R., Siddall B.J., Bell R.A., Kvetnansky R. and Wong D.L. (2007). Stress-induced changes in epinephrine expression in the adrenal medulla in vivo. J. Neurochem. 101, 1108-1118.
98. Tharp G.D. (1975). The role of glucocorticoids in exercise. Med. Sci. Sports 7, 6-11.
99. Thompson P.D., Buchner D., Pina I.L., Balady G.J., Williams M.A., Marcus B.H., Berra K., Blair S.N., Costa F., Franklin B., Fletcher G.F., Gordon N.F., Pate R.R., Rodriguez B.L., Yancey A.K. and Wenger N.K. (2003). Exercise and physical activity in the prevention and treatment of atherosclerotic cardiovascular disease. Circulation 107, 3109-3116.
100. Tomlinson A. and Coupland R.E. (1990). The innervation of the adrenal gland. IV. Innervation of the rat adrenal medulla from birth to old age. A descriptive and quantitative morphometric and biochemical study of the innervation of chromaffin cells and adrenal medullary neurons in Wistar rats. J. Anat. 169, 209-236.
101. Ulrich-Lai Y.M., Figueiredo H.F., Ostrander M.M., Choi D.C., Engeland W.C. and Herman J.P. (2006). Chronic stress induces adrenal hyperplasia and hypertrophy in a subregion-specific manner. Am. J. Physiol. Endocrinol. Metab. 29, E965-E973.
102. Van Praag H., Christie B.R., Sejnowski T.J. and Gage F.H. (1999a). Running enhances neurogenesis, learning and long-term potentiation in mice. Proc. Natl. Acad. Sci. USA 96, 13427-13431.
103. Van Praag H., Kempermann G. and Gage F.H. (1999b). Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 2, 266-270.
104. Van Praag H., Shubert T., Zhao C. and Gage F.H. (2005). Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci. 25, 8680-8685.
105. Vandeputte C., Aiden M.P. and Docherty J.R. (2003). Responsiveness to noradrenaline in aorta from wild-type, nitric oxide synthase-2, nitric oxide synthase-3 and a2A/D-adrenoceptor knockout mice. Eur. J. Pharmacol. 466, 129-136.
106. Villaneueva A.L., Schlosser C., Hopper B., Liu J.H., Hoffman D.I. and Rebar R.W. (1986). Increased cortisol production in women runners. J. Clin. Endocrinol. Metab. 63, 133-136.
107. Walberg J.L., Molé P.A. and Stern J.S. (1982). Effect of swim training on development of obesity in the genetically obese rat. Am. J. Physiol. 242, R204-R211.
108. Warren M.P. and Stiehl A.L. (1999). Exercise and female adolescents: effects on the reproductive and skeletal systems. J. Am. Med. Wom. Assoc. 54, 115-120.
109. Wurtman R.J. (2002). Stress and the adrenocortical control of epinephrine synthesis. Metabolism 51, 11-14.
110. Wurtman R.J. and Axelrod J. (1965). Adrenaline synthesis: control by the pituitarygland and adrenal glucocorticoids. Science 150, 1464-1465.