The effects of chronic and acute physical and psychological Stress on Brain- Derived Neurotrophic Factor in Rats
Subject Areas : Journal of Physical Activity and HormonesSheida Ghanbari Ghooshchi 1 , Maryam Koushkie Jahromi 2
1 - Department of Sport Sciences, School of Education & Psychology, Shiraz University, Iran
2 - Associate Professor in Exercise Physiology, Department of Sport Sciences, International division, Shiraz University, Iran
Keywords: Aerobic exercise, Brain-Derived Neurotrophic Factor, Emotional stress, Physical stress,
Abstract :
Introduction: Different kinds of chronic stress can induce various effects on body systems including the brain. One of the factors related to brain function is brain derived neurotropic factor (BDNF). So, the purpose of the present study was to evaluate the influence of physical stress as aerobic exercise/training and psychological stress on brain derived neurotropic factor (BDNF) in Wistar rats. Material & Methods: The study was semi experimental. 90 healthy male Wistar rats (weight 200±40 gr) were randomly divided in to 6 groups of Exercise (EX), Emotional stress (ES), Physical stress (PS), exercise combined with emotional (EXES), exercise combined with physical stress (EXPS) and control. Wistar rats were exposed to programs included one session (acute) and two weeks (chronic) aerobic training on treadmill with or without emotional and physical stress. Blood samples, for BDNF measurement, were taken 12 hours following the last session of treatment. Statistical tests of analysis of variance and follow up Bonferroni test were used for data analysis. Results: After one session of the experiment, BDNF increased significantly in the EX group compared to other groups (p<0.05). After two weeks of training, BDNF significantly decreased in the ES groups compared to other groups, while BDNF increased in EXES compared to ES (P<0.05) group. One session of EX increased BDNF compared to non-EX groups, but following two weeks, chronic ES per se reduced BDNF compared to non-ES groups. But when ES combined with EX caused increasing of BDNF. Conclusions: Present findings suggest that EX can probably prevent decreasing effect of ES on BDNF. However, future research should clarify the source of BDNF changes.
References
1. Poo MM. Neurotrophins as synaptic modulators. Nat Rev Neurosci 2001; 2: 24-32.
2. Cassiman D, Denef C, Desmet VJ, Roskams T. Human and rat hepatic stellate cells express neurotrophins and neurotrophin receptors. Hepatology 2001; 33: 148-158.
3. Sornelli F, Fiore M, Chaldakov GN, Aloe L. Adipose tissue-derived nerve growth factor and brain-derived neurotrophic factor: results from experimental stress and diabetes. Gen Physiol Biophys 2009; 28: 179-183.
4. Wisse BE, Schwartz MW. The skinny on neurotrophins. Nature Nat Neurosci 2003; 6: 655-656.
5. Pedersen BK, Pedersen M, Krabbe KS, Bruunsgaard H, Matthews VB, Febbraio MA. Role of exercise‐induced brain‐derived neurotrophic factor production in the regulation of energy homeostasis in mammals. Exp Physiol 2009; 94: 1153-1160.
6. Zagrebelsky M, Korte M. Form follows function: BDNF and its involvement in sculpting the function and structure of synapses. Neuropharmacology 2014; 76: 628-638.
7. Noble EE, Billington CJ, Kotz CM, Wang C. The lighter side of BDNF. Am J Physiol Regul Integr Comp Physiol 2011; 300: R1053-R1069.
8. Lommatzsch M, Zingler D, Schuhbaeck K, Schloetcke K, Zingler C, Schuff-Werner P, et al. The impact of age, weight and gender on BDNF levels in human platelets and plasma. Neurobiol Aging 2005; 26: 115-123.
9. Huang T, Larsen KT, Ried-Larsen M, Møller NC, Andersen LB. The effects of physical activity and exercise on brain‐derived neurotrophic factor in healthy humans: A review. Scand J Med Sci Sports 2014; 24: 1-10.
10. Mitoma M, Yoshimura R, Sugita A, Umene W, Hori H, Nakano H, et al. Stress at work alters serum brain-derived neurotrophic factor (BDNF) levels and plasma 3-methoxy-4-hydroxyphenylglycol (MHPG) levels in healthy volunteers: BDNF and MHPG as possible biological markers of mental stress? Prog Neuropsychopharmacol Biol Psychiatry 2008; 32: 679-685.
11. Karege F, Schwald M, Cisse M. Postnatal developmental profile of brain-derived neurotrophic factor in rat brain and platelets. Neurosci Lett 2002; 328: 261-264.
12. Klein AB, Williamson R, Santini MA, Clemmensen C, Ettrup A, Rios M, et al. Blood BDNF concentrations reflect brain-tissue BDNF levels across species. Int J Neuropsychopharmacol 2011; 14: 347-53.
13. Wei M, Gibbons LW, Kampert JB, Nichaman MZ, Blair SN. Low cardiorespiratory fitness and physical inactivity as predictors of mortality in men with type 2 diabetes. Ann Intern Med 2000; 132, 605-611.
14. Lautenschlager NT, Cox KL, Flicker L, Foster JK, van Bockxmeer FM, Xiao J, et al. Effect of physical activity on cognitive function in older adults at risk for Alzheimer disease: a randomized trial. JAMA 2008; 300: 1027-1037.
15. Markser VZ. Sport psychiatry and psychotherapy. Mental strains and disorders in professional sports. Challenge and answer to societal changes. Eur Arch Psychiatry Clin Neurosci 2011; 261: 182-185.
16. Salmon P. Effects of physical exercise on anxiety, depression, and sensitivity to stress: a unifying theory. Clin Psychol Rev 2001; 21: 33-61.
17. McEwen BS. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 2007; 87: 873-904.
18. Stults-Kolehmainen M A, Bartholomew JB, Sinha R. Chronic psychological stress impairs recovery of muscular function and somatic sensations over a 96-hour period. J Strength Cond Res 2014; 28: 2007-2017.
19. Bartholomew JB, Stults-Kolehmainen MA, Elrod CC, Todd JS. Strength gains after resistance training: the effect of stressful, negative life events. J Strength Cond Res 2008; 22: 1215-1221.
20. Stranahan AM, Khalil D, Gould E. Social isolation delays the positive effects of running on adult neurogenesis. Nat Neurosci 2006; 9: 526-533.
21. Wilcox S, King AC. The effects of life events and interpersonal loss on exercise adherence in older adults. J Aging Phys Act 2004; 12: 117-130.
22. Hackney AC. Stress and the neuroendocrine system: the role of exercise as a stressor and modifier of stress. Expert Rev Clin Immunol 2006; 1: 783-792.
23. Stults-Kolehmainen M A, Sinha R. The effects of stress on physical activity and exercise. Sports Med 2014; 44: 81-121.
24. Bath KG, Schilit A, Lee FS. Stress effects on BDNF expression: effects of age, sex, and form of stress. Neuroscience 2013; 239: 149-156.
25. Ieraci A, Mallei A, Musazzi L, Popoli M. Physical exercise and acute restraint stress differentially modulate hippocampal brain‐derived neurotrophic factor transcripts and epigenetic mechanisms in mice. Hippocampus 2015; 25: 1380-1392.
26. US Department of Health and Human Services. NIH Publication No. 86-23, (revised 1985). National Institutes of Health, Bethesda, MD, USA.
27. Brooks GA, White TP. Determination of metabolic and heart rate responses of rats to treadmill exercise. J Appl Physiol 1978; 45: 1009-1015.
28. Scopel D, Fochesatto C, Cimarosti H, Rabbo M, Belló-Klein A, Salbego C, et al. Exercise intensity influences cell injury in rat hippocampal slices exposed to oxygen and glucose deprivation. Brain Res Bull 2006; 71: 155-159.
29. Nofuji Y, Suwa M, Sasaki H, Ichimiya A, Nishichi R, Kumagai S. Different Circulating Brain-Derived Neurotrophic Factor responses to acute exercise between physically active and sedentary subjects. J Sports Sci Med 2012; 11: 83-88.
30. Heyman E, Gamelin FX, Goekint M, Piscitelli F, Roelands B, Leclair E, et al. Intense exercise increases circulating endocannabinoid and BDNF levels in humans possible implications for reward and depression. Psychoneuroendocrinology 2012; 37: 844-851.
31. Zoladz JA, 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: 119-132.
32. Schiffer T, Schulte S, Hollmann W, Bloch W, Strüder HK. Effects of strength and endurance training on brain-derived neurotrophic factor and insulin-like growth factor 1 in humans. Horm Metab Res 2009; 41: 250-254.
33. Rasmussen P, Brassard P, Adser H, Pedersen MV, Leick L, Hart E, et al. Evidence for a release of brain‐derived neurotrophic factor from the brain during exercise. Exp Physiol 2009; 94: 1062-1069.
34. Ruscheweyh R, Willemer C, Krüger K, Duning T, Warnecke T, Sommer J, et al. Physical activity and memory functions: an interventional study. Neurobiol Aging 2011; 32: 1304-1319.
35. Suijo K, Inoue S, Ohya Y, Odagiri Y, Takamiya T, Ishibashi H, et al. Resistance exercise enhances cognitive function in mouse. Int J Sports Med 2013; 34: 368-375.
37. Korte SM. Corticosteroids in relation to fear, anxiety and psychopathology. Neurosci Biobehav Rev2001; 25: 117-142.
38. Powers SK, Locke M, Demirel HA. Exercise, heat shock proteins, and myocardial protection from I-R injury. Med Sci Sports Exerc 2001; 33: 386-392.
39. Sousa N, Lukoyanov NV, Madeira MD, Almeida OF, Paula-Barbosa MM. Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 2000; 97: 253-266.
40. Tsukinoki K, Saruta J, Sasaguri K, Miyoshi Y, Jinbu Y, Kusama M, et al. Immobilization stress induces BDNF in rat submandibular glands. J Dent Res 2006; 85: 844-848.
41. Fujihara H, Sei H, Morita Y, Ueta Y, Morita K. Short-term sleep disturbance enhances brain-derived neurotrophic factor gene expression in rat hippocampus by acting as internal stressor. J Mol Neurosci 2003; 21: 223-231.
42. Murakami S, Imbe H, Morikawa Y, Kubo C, Senba E. Chronic stress, as well as acute stress, reduces BDNF mRNA expression in the rat hippocampus but less robustly. Neurosci Res 2005; 53: 129-139.
43. Duman RS, Monteggia LM. A neurotrophic model for stress-related mood disorders. Biol Psychiatry 2006; 59: 1116-1127.
44. Rasmusson AM, 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.
45. Lin Y, Ter Horst GJ, Wichmann R, Bakker P, Liu A, Li X, et al. Sex differences in the effects of acute and chronic stress and recovery after long-term stress on stress-related brain regions of rats. Cereb Cortex 2009; 19: 1978-1989.
46. Molteni R, Wu A, Vaynman S, Ying Z, Barnard RJ, Gómez-Pinilla F. Exercise reverses the harmful effects of consumption of a high-fat diet on synaptic and behavioral plasticity associated to the action of brain-derived neurotrophic factor. Neuroscience 2004; 123: 429-440.
47. Kwon DH, Kim BS, Chang H, Kim YI, Jo SA, Leem YH. Exercise ameliorates cognition impairment due to restraint stress-induced oxidative insult and reduced BDNF level. Biochem Biophys Res Commun 2013;434: 245-251.
48. Kavushansky A, Ben-Shachar D, Richter-Levin G, Klein E. Physical stress differs from psychosocial stress in the pattern and time-course of behavioral responses, serum corticosterone and expression of plasticity-related genes in the rat. Stress 2009; 12: 412-425.
49. Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci 2006; 9: 519-525.
50. Pacák K, Palkovits M. Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr Rev 2001; 22: 502-548.