Dexmedetomidine ameliorates intracerebral hemorrhage-induced memory impairment by inhibiting apoptosis and enhancing brain-derived neurotrophic factor expression in the rat hippocampus

International Journal of Molecular Medicine

Volumn 31, Issue 5, 2013, Pages 1047-1056

  Hwang, Lakkyong ^a   Choi, In Young ^a   Kim, Sung Eun ^a   Ko, Il Gyu ^a   Shin, Mal Soon ^a   Kim, Chang Ju ^a   Kim, Sang Hoon ^b   Jin, Jun Jang ^c   Chung, Jun Young ^d   Yi, Jae Woo ^d  

^a Kyung Hee University Hospital   (South Korea)

^b Sangmyung University   (South Korea)

^c Hanseo University   (South Korea)

^d Kyung Hee University College of Medicine   (South Korea)

Author keywords

2 adrenoreceptors; Apoptosis; Dexmedetomidine; Intracerebral hemorrhage; Short term memory; Spatial learning memory

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CASPASE 3; DEXMEDETOMIDINE; DNA NUCLEOTIDYLEXOTRANSFERASE; NEUROTROPHIC FACTOR; PROTEIN BAX; PROTEIN BCL 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN HEMORRHAGE; CELL SURVIVAL; CONTROLLED STUDY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MAZE TEST; MEMORY DISORDER; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SHORT TERM MEMORY; SPATIAL LEARNING; SPATIAL MEMORY; TREATMENT DURATION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; AVOIDANCE LEARNING; BCL-2-ASSOCIATED X PROTEIN; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CA1 REGION, HIPPOCAMPAL; CASPASE 3; CEREBRAL HEMORRHAGE; DEXMEDETOMIDINE; DNA FRAGMENTATION; IN SITU NICK-END LABELING; MAZE LEARNING; MEMORY DISORDERS; MEMORY, SHORT-TERM; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, TRKB;

EID: 84876155955     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.2013.1301     Document Type: Article

References (46)

1. Ferro JM: Update on intracerebral haemorrhage. J Neurol 253: 985-999, 2006.
2. Lee HH, Kim H, Lee MH, Chang HK, Lee TH, Jang MH, Shin MC, Lim BV, Shin MS, Kim YP, Yoon JH, Jeong IG and Kim CJ: Treadmill exercise decreases intrastriatal hemorrhage-induced neuronal cell death via suppression on caspase-3 expression in rats. Neurosci Lett 352: 33-36, 2003.
3. Suh HJ, So SM, Na YG, Ko IG, Kim SE, Sung YS, Shin MS, Kim CJ, Cho YS and Kim KH: Neuroprotective effects of tamsulosin on intracerebral hemorrhage. Neural Regen Res 6: 2505-2510, 2011.
4. Thompson CB: Apoptosis in the pathogenesis and treatment of disease. Science 267: 1456-1462, 1995.
5. Johnson EM Jr, Greenlund LJ, Atkins PT and Hsu CY: Neuronal apoptosis: Current understanding of molecular mechanisms and potential role in ischemic brain injury. J Neurotrauma 12: 843-852, 1995.
6. Reed CJ: Apoptosis and cancer: Strategies for integrating programmed cell death. Semin Hematol 37 (Suppl 7): 9-16, 2000.
7. Gong C, Boulis N, Qian J, Turner DE, Hoff JT and Keep RF: Intracerebral hemorrhage-induced neuronal death. Neurosurgery 48: 875-882, 2001.
8. Upadhyay D, Panduri V, Ghio A and Kamp DW: Particulate matter induces alveolar epithelial cell DNA damage and apoptosis: Role of free radicals and the mitochondria. Am J Respir Cell Mol Biol 29: 180-187, 2003.
9. Gomez-Pinilla F and Vaynman S: A 'deficient environment' in prenatal life may compromise systems important for cognitive function by affecting BDNF in the hippocampus. Exp Neurol 192: 235-243, 2005.
10. Minichiello L: TrkB signalling pathways in LTP and learning. Nat Rev Neurosci 10: 850-860, 2009.
11. Zimmerberg B, Foote HE and Van Kempen TA: Olfactory association learning and brain-derived neurotrophic factor in an animal model of early deprivation. Dev Psychobiol 51: 333-344, 2009.
12. Hasegawa Y, Suzuki H, Altay O and Zhang JH: Preservation of tropomyosin-related kinase B (TrkB) signaling by sodium orthovanadate attenuates early brain injury after subarachnoid hemorrhage in rats. Stroke 42: 477-483, 2011.
13. Ard J, Doyle W and Bekker A: Awake craniotomy with dexmedetomidine in pediatric patients. J Neurosurg Anesthesiol 15: 263-266, 2003.
14. Ramsay MA and Luterman DL: Dexmedetomidine as a total intravenous anesthetic agent. Anesthesiology 101: 787-790, 2004.
15. Dahmani S, Rouelle D, Gressens P and Mantz J: Effects of dexmedetomidine on hippocampal focal adhesion kinase tyrosine phosphorylation in physiologic and ischemic conditions. Anesthesiology 103: 969-977, 2005.
16. Laudenbach V, Mantz J, Lagercrantz H, Desmonts JM, Evrard P and Gressens P: Effects of α2-adrenoceptor agonists on perinatal excitotoxic brain injury: Comparison of clonidine and dexmedetomidine. Anesthesiology 96: 134-141, 2002.
17. Ma D, Hossain M, Rajakumaraswamy N, Arshad M, Sanders RD, Franks NP and Maze M: Dexmedetomidine produces its neuroprotective effect via the α2A-adrenoceptor subtype. Eur J Pharmacol 502: 87-97, 2004.
18. Eser O, Fidan H, Sahin O, Cosar M, Yaman M, Mollaoglu H, Songur A and Buyukbas S: The influence of dexmedetomidine on ischemic rat hippocampus. Brain Res 1218: 250-256, 2008.
19. Cosar M, Eser O, Fidan H, Sahin O, Buyukbas S, Ela Y, Yagmurca M and Ozen OA: The neuroprotective effect of dexmedetomidine in the hippocampus of rabbits after subarachnoid hemorrhage. Surg Neurol 71: 54-59, 2009.
20. Ayoglu H, Gul S, Hanci V, Bahadir B, Bektas S, Mungan AG, Turan IO and Acikgoz B: The effects of dexmedetomidine dosage on cerebral vasospasm in a rat subarachnoid haemorrhage model. J Clin Neurosci 17: 770-773, 2010.
21. Hall JE, Uhrich TD, Barney JA, Arain SR and Ebert TJ: Sedative, amnestic, and analgesic properties of small-dose dexmedetomidine infusions. Anesth Analg 90: 699-705, 2000.
22. Takamatsu I, Iwase A, Ozaki M, Kazama T, Wada K and Sekiguchi M: Dexmedetomidine reduces long-term potentiation in mouse hippocampus. Anesthesiology 108: 94-102, 2008.
23. van Oostrom H, Stienen PJ, Doornenbal A and Hellebrekers LJ: The α2-adrenoceptor agonist dexmedetomidine suppresses memory formation only at doses attenuating the perception of sensory input. Eur J Pharmacol 629: 58-62, 2010.
24. Hayama HR, Drumheller KM, Mastromonaco M, Reist C, Cahill LF and Alkire MT: Event-related functional magnetic resonance imaging of a low dose of dexmedetomidine that impairs long-term memory. Anesthesiology 117: 981-995, 2012.
25. Ko IG, Shin MS, Kim BK, Kim SE, Sung YH, Kim TS, Shin MC, Cho HJ, Kim SC, Kim SH, Kim KH, Shin DH and Kim CJ: Tadalafil improves short-term memory by suppressing ischemia-induced apoptosis of hippocampal neuronal cells in gerbils. Pharmacol Biochem Behav 91: 629-635, 2009.
26. Kim SE, Ko IG, Kim BK, Shin MS, Cho S, Kim CJ, Kim SH, Baek SS, Lee EK and Jee YS: Treadmill exercise prevents aging-induced failure of memory through an increase in neurogenesis and suppression of apoptosis in rat hippocampus. Exp Gerontol 45: 357-365, 2010.
27. Nys GM, van Zandvoort MJ, de Kort PL, Jansen BP, de Haan EH and Kappelle LJ: Cognitive disorders in acute stroke: Prevalence and clinical determinants. Cerebrovasc Dis 23: 408-416, 2007.
28. Su CY, Chen HM, Kwan AL, Lin YH and Guo NW: Neuro-psychological impairment after hemorrhagic stroke in basal ganglia. Arch Clin Neuropsychol 22: 465-474, 2007.
29. Ko IG, Cho H, Kim SE, Kim JE, Sung YH, Kim BK, Shin MS, Cho S, Pak YK and Kim CJ: Hypothermia alleviates hypoxic ischemia-induced dopamine dysfunction and memory impairment in rats. Anim Cells Syst 15: 279-286, 2011.
30. Baek SS, Jun TW, Kim KJ, Shin MS, Kang SY and Kim CJ: Effects of postnatal treadmill exercise on apoptotic neuronal cell death and cell proliferation of maternal-separated rat pups. Brain Dev 34: 45-56, 2012.
31. Matsushita K, Meng W, Wang X, Asahi M, Asahi K, Moskowitz MA and Lo EH: Evidence for apoptosis after intercerebral hemorrhage in rat striatum. J Cereb Blood Flow Metab 20: 396-404, 2000.
32. Qureshi AI: Nonsteroidal anti-inflammatory drugs and the risk of intracerebral hemorrhage. Stroke 34: 379-386, 2003.
33. Benchoua A, Braudeau J, Reis A, Couriaud C and Onténiente B: Activation of proinflammatory caspases by cathepsin B in focal cerebral ischemia. J Cereb Blood Flow Metab 24: 1272-1279, 2004.
34. Plesnila N, Zinkel S, Amin-Hanjani S, Qiu J, Korsmeyer SJ and Moskowitz MA: Function of BID-a molecule of the bcl-2 family-in ischemic cell death in the brain. Eur Surg Res 34: 37-41, 2002.
35. Niizuma K, Endo H, Nito C, Myer DJ, Kim GS and Chan PH: The PIDDosome mediates delayed death of hippocampal CA1 neurons after transient global cerebral ischemia in rats. Proc Natl Acad Sci USA 105: 16368-16373, 2008.
36. Sugawara T, Fujimura M, Noshita N, Kim GW, Saito A, Hayashi T, Narasimhan P, Maier CM and Chan PH: Neuronal death/survival signaling pathways in cerebral ischemia. NeuroRx 1: 17-25, 2004.
37. Kuwana T and Newmeyer DD: Bcl-2-family proteins and the role of mitochondria in apoptosis. Curr Opin Cell Biol 15: 691-699, 2003.
38. Engelhard K, Werner C, Eberspächer E, Bachl M, Blobner M, Hildt E, Hutzler P and Kochs E: The effect of the α2-agonist dexmedetomidine and the N-methyl-D-aspartate antagonist S(+)ketamine on the expression of apoptosis-regulating proteins after incomplete cerebral ischemia and reperfusion in rats. Anesth Analg 96: 524-531, 2003.
39. Il'inykh FA, Bannova AV, Kalinina TS and Dygalo NN: Effects of ligands of α2-adrenoceptors on mRNA level of apoptotic proteins in the developing rat brain. Izv Akad Nauk Ser Biol 1: 104-109, 2008 (In Russian).
40. Sanders RD, Sun P, Patel S, Li M, Maze M and Ma D: Dexmedetomidine provides cortical neuroprotection: Impact on anaesthetic-induced neuroapoptosis in the rat developing brain. Acta Anaesthesiol Scand 54: 710-716, 2010.
41. Xu B, Gottschalk W, Chow A, Wilson RI, Schnell E, Zang K, Wang D, Nicoll RA, Lu B and Reichardt LF: The role of brain-derived neurotrophic factor receptors in the mature hippocampus: Modulation of long-term potentiation through a presynaptic mechanism involving TrkB. J Neurosci 20: 6888-6897, 2000.
42. Pang PT, Teng HK, Zaitsev E, Woo NT, Sakata K, Zhen S, Teng KK, Yung WH, Hempstead BL and Lu B: Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 306: 487-491, 2004.
43. Hellmich HL, Garcia JM, Shimamura M, Shah SA, Avila MA, Uchida T, Parsley MA, Capra BA, Eidson KA, Kennedy DR, Winston JH, DeWitt DS and Prough DS: Traumatic brain injury and hemorrhagic hypotension suppress neuroprotective gene expression in injured hippocampal neurons. Anesthesiology 102: 806-814, 2005.
44. Sairanen M, Lucas G, Ernfors P, Castrén M and Castrén E: Brain-derived neurotrophic factor and antidepressant drugs have different but coordinated effects on neuronal turnover, proliferation, and survival in the adult dentate gyrus. J Neurosci 25: 1089-1094, 2005.
45. Suzuki A, Fukushima H, Mukawa T, Toyoda H, Wu LJ, Zhao MG, Xu H, Shang Y, Endoh K, Iwamoto T, Mamiya N, Okano E, Hasegawa S, Mercaldo V, Zhang Y, Maeda R, Ohta M, Josselyn SA, Zhuo M and Kida S: Upregulation of CREBmediated transcription enhances both short-and long-term memory. J Neurosci 31: 8786-8802, 2011.
46. Han QQ, Jin W, Xiao ZF, Huang JC, Ni HB, Kong J, Wu J, Chen B, Liang WB and Dai JW: The promotion of neurological recovery in an intracerebral hemorrhage model using fibrin-binding brain derived neurotrophic factor. Biomaterials 32: 3244-3252, 2011.