Assessment of oxidative stress parameters of brain-derived neurotrophic factor heterozygous mice in acute stress model

Document Type: Original Article

Authors

1 Department of Physiology, Faculty of Medicine, Giresun University, Turkey

2 Department of Clinical Biochemistry, Faculty of Medicine, Karadeniz Technical University, Turkey

Abstract

Objective(s): Exposing to stress may be associated with increased production of reactive oxygen species (ROS). Therefore, high level of oxidative stress may eventually give rise to accumulation of oxidative damage and development of numerous neurodegenerative diseases. It has been presented that brain-derived neurotrophic factor (BDNF) supports neurons against various neurodegenerative conditions. Lately, there has been growing evidence that changes in the cerebral neurotrophic support and especially in the BDNF expression and its engagement with ROS might be important in various disorders and neurodegenerative diseases. Hence, we aimed to investigate protective effects of BDNF against stress-induced oxidative damage.
Materials and Methods: Five- to six-month-old male wild-type and BDNF knock-down mice were used in this study. Activities of catalase (CAT) and superoxide dismutase (SOD) enzymes, and the amount of malondialdehyde (MDA) were assessed in the cerebral homogenates of studied groups in response to acute restraint stress.
Results: Exposing to acute physiological stress led to significant elevation in the markers of oxidative stress in the cerebral cortexes of experimental groups.
Conclusion: As BDNF-deficient mice were observed to be more susceptible to stress-induced oxidative damage, it can be suggested that there is a direct interplay between oxidative stress indicators and BDNF levels in the brain.

Keywords


1. Hong IS, Lee HY, Kim HP. Anti-oxidative effects of Rooibos tea (Aspalathus linearis) on immobilization-induced oxidative stress in rat brain. PLoS One 2014; 21 9:e87061.

2. Kelly GS. Nutritional and botanical interventions to assist with the adaptation to stress. Altern Med Rev 1999; 4:249-265.

3. Liu J, Mori A. Stress, aging, and brain oxidative damage. Neurochem Res 1999; 24:1479-1497.

4. Uttara B, Singh AV, Zamboni P, Mahajan RT. Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol 2009; 7:65-74.

5. Huang EJ, Reichardt LF. Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 2003; 72:609-642.

6. Numakawa T, Suzuki S, Kumamaru E, Adachi N, Richards M, Kunugi H. BDNF function and intracellular signaling in neurons. Histol Histopathol 2010; 25:237-258.

7. Vedunova MV, Mishchenko TA, Mitroshina EV, Mukhina IV. TrkB-mediated neuroprotective and antihypoxic properties of brain-derived neurotrophic factor. Oxid Med Cell Longev 2015; 2015:453901.

8. Numakawa T, Matsumoto T, Numakawa Y, Richards M, Yamawaki S, Kunugi H. Protective action of neurotrophic factors and estrogen against oxidative stress-mediated neurodegeneration. J Toxicol 2011; 2011:405194.

9. Ferrer I, Goutan E, Marín C, Rey MJ, Ribalta T. Brain-derived neurotrophic factor in Huntington disease.  Brain Res 2000; 866:257-261.

10. Gines S, Seong IS, Fossale E, Ivanova E, Trettel F, Gusella JF, et al. Specific progressive cAMP reduction implicates energy deficit in presymptomatic Huntington's disease knock-in mice. Hum Mol Genet 2003; 12:497-508.

11. Counts SE, Mufson EJ. Noradrenaline activation of neurotrophic pathways protects against neuronal amyloid toxicity. J Neurochem 2010; 113:649-660.

12. Giese M, Unternaehrer E, Brand S, Calabrese P, Holsboer-Trachsler E, Eckert A. The interplay of stress and sleep impacts BDNF level. PLoS One 2013; 16 8(10):e76050.

13. Aydemir O, Deveci A. BDNF measurement in stress-related mood disorders: a review of clinical studies. Turk Psikiyatri Derg 2009; 20:385-391.

14. Duman RS. Pathophysiology of depression: the concept of synaptic plasticity. Eur Psychiatry 2002; 17:306S-310S.

15. Pae CU, Chiesa A, Porcelli S, Han C, Patkar AA, Lee SJ, et al. Influence of BDNF variants on diagnosis and response to treatment in patients with major depression, bipolar disorder and schizophrenia. Neuropsychobiology 2011; 65:1-11.

16. Haghighi M, Salehi I, Erfani P, Jahangard L, Bajoghli H, Holsboer-Trachsler E, et al. Additional ECT increases BDNF-levels in patients suffering from major depressive disorders compared to patients treated with citalopram only. J Psychiatr Res 2013; 47:908-915.

17. Hosang GM, Shiles C, Tansey KE, McGuffin P, Uher R. Interaction between stress and the BDNF Val66Met polymorphism in depression: a systematic review and meta-analysis. BMC Med 2014; 16 12:7.

18. Tsuru J, Tanaka Y, Ishitobi Y, Maruyama Y, Inoue A, Kawano A, et al. Association of BDNF Val66Met polymorphism with HPA and SAM axis reactivity to psychological and physical stress. Neuropsychiatr Dis Treat 2014; 11:2123-2133.

19. Burke TF, Advani T, Adachi M, Monteggia LM, Hensler JG. Sensitivity of hippocampal 5-HT1A receptors to mild stress in BDNF-deficient mice. Int J Neuropsychopharmacol 2013; 16:631-645.

20. Korte M, Carroll P, Wolf E, Brem G, Thoenen H, Bonhoeffer T. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci U S A 1995; 92:8856-8860.

21. Abidin I, Eysel UT, Lessmann V, Mittmann T. Impaired GABAergic inhibition in the visual cortex of brain-derived neurotrophic factor heterozygous knockout mice. J Physiol 2008; 586:1885-1901.

22. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72:248-254.

23. Uchiyama M, Mihara M. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 1978; 86:271-278.

24. Sun Y, Oberley LW, Li Y. A simple method for clinical assay of superoxide dismutase. Clin Chem 1988; 34:497-500.

25. Goth L. A simple method for determination of serum catalase activity and revision of reference range. Clin Chim Acta 1991; 196:143-151.

26. Palmieri B, Sblendorio V. Oxidative stress tests: overview on reliability and use. Part II Eur Rev Med Pharmacol Sci 2007; 11:383-399.

27. Landis GN, Tower J. Superoxide dismutase evolution and life span regulation. Mech Ageing Dev 2005; 126:365-379.

28. Al-Abrash AS, Al-Quobaili FA, Al-Akhras GN. Catalase evaluation in different human diseases associated with oxidative stress. Saudi Med J 2000; 21:826-830.

29. Abidin I, Köhler T, Weiler E, Zoidl G, Eysel UT, Lessmann V, et al. Reduced presynaptic efficiency of excitatory synaptic transmission impairs LTP in the visual cortex of BDNF-heterozygous mice. Eur J Neurosci 2006; 24:3519-3531.

30. Sahin E, Gümü┼člü S. Immobilization stress in rat tissues: alterations in protein oxidation, lipid peroxidation and antioxidant defense system. Comp Biochem Physiol C Toxicol Pharmacol 2007; 144:342-347.

31. Laugero KD, Moberg GP. Energetic response to repeated restraint stress in rapidly growing mice. Am J Physiol Endocrinol Metab 2000; 279:33-43.

32. Lehmann J, Russig H, Feldon J, Pryce CR. Effect of a single maternal separation at different pup ages of the corticosterone stress response in adult and aged rats. Pharmacol Biochem Behav 2002; 73:141-145.

33. Djordjevic J, Cvijic G, Davidovic V. Different activation of ACTH and corticosterone release in response to various stressors in rats. Physiol Res 2003; 52:67-72.

34. Fontella FU, Siqueira IR, Vasconcellos AP, Tabajara AS, Netto CA, Dalmaz C. Repeated restraint stress induces oxidative damage in rat hippocampus. Neurochem Res. 2005; 30:105-111.

35. Singh LK, Rang X, Alexacos N, Netaumen R. Theoharides, acute immobilization stress triggers skin mast cell degranulation via corticotropin releasing hormone neurotension and substance link to neurogenic skin disorders.  Brain Behav Immunol 1993; 3:225-239.

36. Ramanova TP, Karpel GG, Brill GF, Markow KM. Mechanism of disorders of the cerebral blood supply during stress in spontaneously hypertensive rats. Pathol Fiziol Exp Ter 1994; 3:5-8.

37. Maestre I, Jordan J, Calvo S, Reig JA, Cena V, Soria B, et al. Mitochondrial dysfunction is involved in apoptosis induced by serum withdrawal and fatty acids in the beta-cell line INS-1. Endocrinology 2003; 144:335-345.

38. Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 1991; 11:81-128.

39. Kapczinski F, Frey BN, Andreazza AC, Kauer-Sant'Anna M, Cunha AB, Post RM. Increased oxidative stress as a mechanism for decreased BDNF levels in acute manic episodes. Rev Bras Psiquiatr 2008; 30:243-245.

40. Gama CS, Berk M, Andreazza AC, Kapczinski F, Belmonte-de-Abreu P. Serum levels of brain-derived neurotrophic factor and thiobarbituric acid reactive
substances in chronically medicated schizophrenic patients: a positive correlation. Rev Bras Psiquiatr 2008; 30:337-340.

41. Posmyk MM, Bailly C, Szafranska K, Janas KM, Corbineau F.  Antioxidant enzymes and isoflavonoids in chilled soybean (Glycine max (L.) Merr.) seedlings. J Plant Physiol 2005; 162:403-412.

42. Zhang XY, Chen DC, Tan YL, Tan Shu-ping, Wang ZR, Yang FD, et al. The interplay between BDNF and oxidative stress in chronic schizophrenia.  Psychoneuroendocrinology 2015; 51:201-208. 

43. Yao JK, Reddy R, McElhinny LG, van Kammen DP. Reduced status of plasma total antioxidant capacity in schizophrenia. Schizophr Res 1998; 32:1-8.

44. Zhang XY, Zhou DF, Zhang PY, Wu GY, Su JM, Cao LY. A double-blind, placebo-controlled trial of extract of Ginkgo biloba added to haloperidol in treatment-resistant patients with schizophrenia. J Clin Psychiatry 2001; 62:878-883.