Effect Of Envıronmental Enrıchment On Depressıon-Lıke Behavıor, Cortıcal And Hıppocampal BDNF And IL-1 β In Vascular Dementıa Model

Öz

 Aim: This study was designed to investigate the effects of environmental enrichment (EE) on depressive like-behaviour, and cerebral cortex and hippocampus brain derived neurotrophic factor (BDNF), IL-1β and caspase-1 levels in vascular dementia model induced by chronic cerebral hypoperfusion (CCH). Previous studies demonstrated that EE posesses beneficial effects againts CCH including inhibition oxidative stress and stimulation of endogenous neuroprotective factors. 

Material and Methods: CCH was induced by permanent occlusion of the bilateral common carotid arteries in rats. Animals were divided into three groups: Sham control, standart cage condition and enriched condition for 4 weeks. Sucrose preference and forced swiming test (FST) were used for evaluation of depressive like behaviour after induction of CCH.   The change in BDNF, IL-1β and caspase-1 levels were also examined. 

Results: CCH caused a decrease in the hippocampus BDNF level and depressive behaviour associated with increase in IL-1β and caspase-1 levels. EE attenuated depressive behaviour by preserving BDNF level and reducing inflammatory response in hippocampus. 

Conclusion: In conclusion, EE may be a new non-pharmacological strategy for ameliorating depressive like behaviour through reducing inflammatory response and restore BDNF levels in cerebral hypoperfusion condition.

Anahtar Kelimeler

• environmental enrichment,depressive like behaviour,BDNF,vascular dementia

Proje Numarası

2016-26259946-01

Vasküler Demans Modelinde Çevresel Zenginleştirmenin Depresyon Benzeri Davranış, Kortikal ve Hipokampal BDNF ve IL-1β Seviyeleri Üzerine Etkisi

Öz

Amaç: Bu çalışma çevresel zenginleştirmenin (EE) kronik serebral hipoperfüzyonla (KSH) oluşturulan vasküler demans modelinde depresyon benzeri davranış, serebral korteks ve hipokampüsde beyin kaynaklı nörotrofik faktör (BDNF), kaspaz-1 ve IL-1β seviyeleri üzerine etkisini incelemek için tasarlanmıştır. Daha önceki çalışmalar EE’nin KSH modelinde oksidatif stres inhibisyonu ve endojen nörokoruyucu faktörlerin artırılmasını içeren yararlı etkilere sahip olduğunu göstermişlerdir. 

Gereç ve Yöntemler: KSH sıçanlarda bilateral ortak karotid arterlerin oklüzyonu ile oluşturulmuştur. Hayvanlar 3 gruba ayrılmıştır: Sham, standart kafes koşulları ve 4 hafta boyunca zenginleştirilmiş koşullara maruz bırakılan grup. Sükroz tercih testi ve zorlu yüzme testi (FST) KSH sonrası depresif davranışı değerlendirmek için kullanılmıştır. BDNF, IL-1β ve kaspaz-1 düzeylerindeki değişim incelenmiştir. 

Bulgular: KSH, hipokampüsde BDNF seviyesinde azalmaya, IL-1β ve kaspaz-1 düzeylerinde artış ile birlikte depresyon benzeri davranışa neden olmuştur.. 

Sonuç: EE serebral hipoperfüzyon durumunda inflamatuar yanıtı azaltarak ve BDNF seviyelerini koruyarak depresif davranışı iyileştirmede farmakolojik olmayan yeni bir strateji olabilir.

Anahtar Kelimeler

• çevresel zenginleştirme,vasküler demans,BDNF,depresif davranış

Destekleyen Kurum

Zonguldak Bülent Ecevit Üniversitesi Bilimsel Araştırma Projeleri Koordinatörlüğü

Proje Numarası

2016-26259946-01

Kaynakça

1. 1. Kasparová S, Brezová V, Valko M, Horecký J, Mlynárik V, Liptaj T, Vancová O, Ulicná O, Dobrota D. Study of the oxidative stress in a rat model of chronic brain hypoperfusion. Neurochem Int. 2005; 46(8):601-11.
2. 2. Cechetti F, Pagnussat AS, Worm PV, Elsner VR, Ben J, da Costa MS, Mestriner R, Weis SN, Netto CA. Chronic brain hypoperfusion causes early glial activation and neuronal death, and subsequent long-term memory impairment. Brain Res Bull. 2012; 87(1):109-16.
3. 3. Saggu R, Schumacher T, Gerich F, Rakers C, Tai K, Delekate A, Petzold GC. Astroglial NF-kB contributes to white matter damage and cognitive impairment in a mouse model of vascular dementia. Acta Neuropathol Commun. 2016; 4(1):76.
4. 4. Ozacmak HS, Ozacmak VH, Turan I. Ethyl pyruvate prevents from chronic cerebral hypoperfusion via preserving cognitive function and decreasing oxidative stress, caspase 3 activation and IL-1β level. Bratisl Lek Listy. 2018;119(8):469-475.
5. 5. Kim JH, Ko PW, Lee HW, Jeong JY, Lee MG, Kim JH, Lee WH, Yu R, Oh WJ, Suk K. Astrocyte-derived lipocalin-2 mediates hippocampal damage and cognitive deficits in experimental models of vascular dementia. Glia 2017; 65(9):1471-1490.
6. 6. He XL, Wang YH, Bi MG, Du GH. Chrysin improves cognitive deficits and brain damage induced by chronic cerebral hypoperfusion in rats. Eur J Pharmacol. 2012; 680(1-3):41-8.
7. 7. Fu X, Zhang J, Guo L, Xu Y, Sun L, Wang S, Feng Y, Gou L, Zhang L, Liu Y Protective role of luteolin against cognitive dysfunction induced by chronic cerebral hypoperfusion in rats. Pharmacol Biochem Behav. 2014; 126:122-30.
8. 8. Hei Y, Chen R, Yi X, Long Q, Gao D, Liu W. HMGB1 Neutralization Attenuates Hippocampal Neuronal Death and Cognitive Impairment in Rats with Chronic Cerebral Hypoperfusion via Suppressing Inflammatory Responses and Oxidative Stress. Neuroscience 2018; 383:150-159.

9. 9. Lee SR, Choi B, Paul S, Seo JH, Back DB, Han JS, Choi DH, Kwon KJ, Shin CY, Lee J, Han SH, Kim HY. Depressive-like behaviors in a rat model of chronic cerebral hypoperfusion. Transl Stroke Res. 2015; 6(3):207-14.
10. 10. Valkanova V, Ebmeier KP. Vascular risk factors and depression in later life: a systematic review and meta-analysis. Biol Psychiatry. 2013; 73(5):406-13.
11. 11. O'Keefe LM, Doran SJ, Mwilambwe-Tshilobo L, Conti LH, Venna VR, McCullough LD. Social isolation after stroke leads to depressive-like behavior and decreased BDNF levels in mice. Behav Brain Res. 2014; 260:162-70.
12. 12. Zhou XY, Zhang F, Hu XT, Chen J, Tang RX, Zheng KY, Song YJ. Depression can be prevented by astaxanthin through inhibition of hippocampal inflammation in diabetic mice. Brain Res. 2017; 1657:262-268.
13. 13. Nabavi SF, Dean OM, Turner A, Sureda A, Daglia M, Nabavi SM. Oxidative stress and post-stroke depression: possible therapeutic role of polyphenols? Curr Med Chem. 2015;22(3):343-51.
14. 14. Ramírez-Rodríguez G, Ocaña-Fernández MA, Vega-Rivera NM, Torres-Pérez OM, Gómez-Sánchez A, Estrada-Camarena E, Ortiz-López L. Environmental enrichment induces neuroplastic changes in middle age female Balb/c mice and increases the hippocampal levels of BDNF, p-Akt and p-MAPK1/2. Neurosciencem 2014; 260:158-70.
15. 15. Dandi Ε, Kalamari A, Touloumi O, Lagoudaki R, Nousiopoulou E, Simeonidou C, Spandou E, Tata DA. Beneficial effects of environmental enrichment on behavior, stress reactivity and synaptophysin/BDNF expression in hippocampus following early life stress. Int J Dev Neurosci. 2018; 67: 19-32.
16. 16. Bayat M, Sharifi MD, Haghani M, Shabani M. Enriched environment improves synaptic plasticity and cognitive deficiency in chronic cerebral hypoperfused rats. Brain Res Bull. 2015; 119(Pt A):34-40.
17. 17. Mahati K, Bhagya V, Christofer T, Sneha A, Shankaranarayana Rao BS. Enriched environment ameliorates depression-induced cognitive deficits and restores abnormal hippocampal synaptic plasticity. Neurobiol Learn Mem. 2016; 134 Pt B:379-91.
18. 18. Park JM, Seong HH, Jin HB, Kim YJ. The Effect of Long-Term Environmental Enrichment in Chronic Cerebral Hypoperfusion-Induced Memory Impairment in Rats. Biol Res Nurs. 2017; 19(3):278-286.
19. 19. Hase Y, Craggs L, Hase M, Stevenson W, Slade J, Chen A, Liang D, Ennaceur A, Oakley A, Ihara M, Horsburgh K, Kalaria RN. The effects of environmental enrichment on white matter pathology in a mouse model of chronic cerebral hypoperfusion. J Cereb Blood Flow Metab. 2018; 38(1):151-165.
20. 20. Barros W, David M, Souza A, Silva M, Matos R. Can the effects of environmental enrichment modulate BDNF expression in hippocampal plasticity? A systematic review of animal studies. Synapse 2019; 73(8):1-15.
21. 21. Chen HH, Zhang N, Li WY, Fang MR, Zhang H, Fang YS, Ding MX, Fu XY. Overexpression of brain-derived neurotrophic factor in the hippocampus protects against post-stroke depression. Neural Regen Res. 2015; 10(9):1427-32.
22. 22. Gao L, Liu X, Yu L, Wu J, Xu M, Liu Y. Folic acid exerts antidepressant effects by upregulating brain-derived neurotrophic factor and glutamate receptor 1 expression in brain. Neuroreport 2017; 28(16):1078-1084.
23. 23. Sun H, Zhang J, Zhang L, Liu H, Zhu H, Yang Y. Environmental enrichment influences BDNF and NR1 levels in the hippocampus and restores cognitive impairment in chronic cerebral hypoperfused rats. Curr Neurovasc Res. 2010; 7(4):268-80.
24. 24. Ghosal S, Bang E, Yue W, Hare BD, Lepack AE, Girgenti MJ, Duman RS. Activity-Dependent Brain-Derived Neurotrophic Factor Release Is Required for the Rapid Antidepressant Actions of Scopolamine. Biol Psychiatry. 2018; 83(1):29-37.
25. 25. Zhang XQ, Mu JW, Wang HB, Jolkkonen J, Liu TT, Xiao T, Zhao M, Zhang CD, Zhao CS. Increased protein expression levels of pCREB, BDNF and SDF-1/CXCR4 in the hippocampus may be associated with enhanced neurogenesis induced by environmental enrichment. Mol Med Rep. 2016; 14(3):2231-7.
26. 26. Nagasawa M, Otsuka T, Yasuo S, Furuse M. Chronic imipramine treatment differentially alters the brain and plasma amino acid metabolism in Wistar and Wistar Kyoto rats. Eur J Pharmacol. 2015; 762:127-35.
27. 27. Santiago RM, Tonin FS, Barbiero J, Zaminelli T, Boschen SL, Andreatini R, Da Cunha C, Lima MM, Vital MA. The nonsteroidal antiinflammatory drug piroxicam reverses the onset of depressive-like behavior in 6-OHDA animal model of Parkinson's disease. Neuroscience 2015;300:246-53.
28. 28. Farkas E, Luiten PG, Bari F. Permanent, bilateral common carotid artery occlusion in the rat: A model for chronic cerebral hypoperfusion-related neurodegenerative diseases. Brain Res Rev 2007; 54: 162–180.
29. 29. Farkas E, Donka G, de Vos RA, Mihály A, Bari F, Luiten PG. Experimental cerebral hypoperfusion induces white matter injury and mi-croglial activation in the rat brain. Acta Neuropathol 2004; 108: 57–64.
30. 30. Ozacmak VH1, Sayan-Ozacmak H1, Barut F1.Chronic treatment with resveratrol, a natural polyphenol found in grapes, alleviates oxidative stress and apoptotic cell death in ovariectomized female rats subjected to chronic cerebral hypoperfusion. Nutr Neurosci. 2016 May;19(4):176-86.
31. 31. Alexopoulos GS. The vascular depression hypothesis: 10 years later. Biol Psychiatry. 2006; 60(12):1304–5.
32. 32. Tiemeier H, van Dijck W, Hofman A, Witteman JC, Stijnen T, Breteler MM. Relationship between atherosclerosis and late-life de-pression: the Rotterdam Study. Arch Gen Psychiatry. 2004; 61(4):369–76.
33. 33. Wang H, Li Q, Tang H, Ding J, Xu N, Sun S, Chen S.The activated newborn neurons participate in enriched environment induced improvement of locomotor function in APP/PS1 mice. Brain Behav. 2019; 9:1-8.
34. 34. Anisman H, Matheson K. Stress, depression, and anhedonia: caveats concerning animal models. Neurosci Biobehav Rev. 2005;29(4–5):525–46.
35. 35. Tang J, Liang X, Zhang Y, Chen L, Wang F, Tan C, Luo Y, Xiao Q, Chao F, Zhang L, Gao Y, Huang C, Qi Y, Tang Y. The effects of running exercise on oligodendrocytes in the hippocampus of rats with depression induced by chronic unpredictable stress. Brain Res Bull. 2019; 149:1-10
36. 36. Zhang C, Zhang YP, Li YY, Liu BP, Wang HY, Li KW, Zhao S, Song C. Minocycline ameliorates depressive behaviors and neuro-immune dysfunction induced by chronic unpredictable mild stress in the rat. Behav Brain Res. 2019; 356:348-357.
37. 37. Hashimoto K. Brain-derived neurotrophic factor as a biomarker for mood disorders: an historical overview and future directions. Psychiatry Clin. Neurosci. 2010; 64: 341-357.
38. 38. Wook Koo J, Labonte B, Engmann O, Calipari ES, Juarez B, Lorsch Z, Walsh ZZ. Essential role of mesolimbic brain-derived neurotrophic factor in chronic social stress-induced depressive behaviors. Biol. Psychiatry 2016; 80: 469-478.
39. 39. Zhang YP, Wang HY, Zhang C, Liu BP, Peng ZL, Li YY, Liu FM, Song C. Mifepristone attenuates depression-like changes induced by chronic central administration of interleukin-1β in rats. Behav Brain Res. 2018; 347:436-445.
40. 40. Magami S, Miyamoto N, Ueno Y, Hira K, Tanaka R, Yamashiro K, Oishi H, Arai H1, Urabe T, Hattori N.The Effects of Astrocyte and Oligodendrocyte Lineage Cell Interaction on White Matter Injury under Chronic Cerebral Hypoperfusion. Neuroscience. 2019; 406:167-175.
41. 41. Shen J, Li Y, Qu C, Xu L, Sun H, Zhang J. The enriched environment ameliorates chronic unpredictable mild stress-induced depressive-like behaviors and cognitive impairment by activating the SIRT1/miR-134 signaling pathway in hippocampus. J Affect Disord. 2019; 248: 81-90.
42. 42. Zhou Y, Zhang J, Wang L. Interleukin-1beta impedes oligodendrocyte progenitor cell recruitment and white matter repair following chronic cerebral hypoperfusion. Brain Behav Immun. 2017; 60: 93–105.
43. 43. Ransohoff RM. How neuroinflammation contributes to neurodegeneration. Science 2016; 353: 777–783.
44. 44. Wang QG, Xue X, Yang Y, Gong PY, Jiang T, Zhang YD. Angiotensin IV suppresses inflammation in the brains of rats with chronic cerebral hypoperfusion. J Renin Angiotensin Aldosterone Syst. 2018; 19(3):1-7.
45. 45. Shaftel SS, Griffin WS, O'Banion MK. The role of interleukin-1 in neuroinflammation and Alzheimer disease: an evolving perspective. J Neuroinflammation 2008; 5:1-12.
46. 46. Fernandes J, Gupta GL. N-acetylcysteine attenuates neuroinflammation associated depressive behavior induced by chronic unpredictable mild stress in rat. Behav Brain Res. 2019;364:356-365.
47. 47. Raison CL, Capuron L, Miller, AH. Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends Immunol. 2006; 27(1):24-31.
48. 48. Liu W, Ge T, Leng Y, Pan Z, Fan J, Yang W, Cui R. The Role of Neural Plasticity in Depression: From Hippocampus to Prefrontal Cortex. Neural Plast. 2017;2017:1-11
49. 49. Hu MZ, Wang AR, Zhao ZY, Chen XY, Li YB, Liu B. Antidepressant-like effects of paeoniflorin on post-stroke depression in a rat model. Neurol Res. 2019; 41(5):446-455.