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Hypothermia alleviates hypoxic ischemia-induced dopamine dysfunction and memory impairment in rats

  • Ko, Il-Gyu (Graduate School of Health Promotion, Hanseo University, Department of Exercise physiology & Prescription) ;
  • Cho, Han-Jin (Korea University Ansan Hospital, Department of Emergency Medicine) ;
  • Kim, Sung-Eun (College of Medicine, Kyung Hee University, Department of Physiology) ;
  • Kim, Ji-Eun (College of Medicine, Kyung Hee University, Department of Physiology) ;
  • Sung, Yun-Hee (College of Medicine, Kyung Hee University, Department of Physiology) ;
  • Kim, Bo-Kyun (College of Medicine, Kyung Hee University, Department of Physiology) ;
  • Shin, Mal-Soon (College of Medicine, Kyung Hee University, Department of Physiology) ;
  • Cho, Seh-Yung (College of Medicine, Kyung Hee University, Department of Physiology) ;
  • KimPak, Young-Mi (College of Medicine, Kyung Hee University, Department of Physiology) ;
  • Kim, Chang-Ju (College of Medicine, Kyung Hee University, Department of Physiology)
  • Received : 2011.03.29
  • Accepted : 2011.06.23
  • Published : 2011.12.31

Abstract

Hypoxic ischemia injury is a common cause of functional brain damage, resulting from a decrease in cerebral blood flow and oxygen supply to the brain. The main problems associated with hypoxic ischemia to the brain are memory impairment and dopamine dysfunction. Hypothermia has been suggested to ameliorate the neurological impairment induced by various brain insults. In this study, we investigated the effects of hypothermia on memory function and dopamine synthesis following hypoxic ischemia to the brain in rats. For this purpose, a step-down avoidance task, a radial eight-arm maze task, and immunohistochemistry for tyrosine hydroxylase (TH) and 5-bromo-2'-deoxyuridine (BrdU) were performed. The present results indicated that the hypoxic ischemia-induced disturbance of the animal's performances and spatial working memory was associated with a decrement in TH expression in the substantia nigra and striatum, and an increase in cell proliferation in the hippocampal dentate gyrus. Hypothermia treatment improved the animals' performance and spatial working memory by suppressing the decrement in TH expression in the substantia nigra and striatum and the increase in cell proliferation in the dentate gyrus. We suggest that hypothermia can be an efficient therapeutic modality to facilitate recovery following hypoxic ischemia injury to the brain, presumably by modulating the dopaminergic cell loss.

Keywords

References

  1. Alva N, Carbonell T, Palomeque J. 2010. Hypothermic protection in an acute hypoxia model in rats: Acid-base and oxidant/antioxidant profiles. Resuscitation. 81: 609-616. https://doi.org/10.1016/j.resuscitation.2010.01.023
  2. Anderson CA, Arciniegas DB. 2010. Cognitive sequelae of hypoxic-ischemic brain injury. NeuroRehabilitation. 26: 47-63.
  3. Asanuma M, Miyazaki I, Ogawa N. 2003. Dopamine- or L-DOPA-induced neurotoxicity: the role of dopamine quinone formation and tyrosinase in a model of Parkinson's disease. Neurotox Res. 5:165-176. https://doi.org/10.1007/BF03033137
  4. Bales JW, Wagner AK, Kline AE, Dixon CE. 2009. Persistent cognitive dysfunction after traumatic brain injury: A dopamine hypothesis. Neurosci Biobehav Rev. 33: 981-1003. https://doi.org/10.1016/j.neubiorev.2009.03.011
  5. Bales JW, Yan HQ, Ma X, Li Y, Samarasinghe R, Dixon CE. 2011. The dopamine and cAMP regulated phosphoprotein, 32kDa (DARPP-32) signaling pathway: a novel therapeutic target in traumatic brain injury. Exp Neurol. 229:300-207. https://doi.org/10.1016/j.expneurol.2011.02.013
  6. Banasiak KJ, Xia Y, Haddad GG. 2000. Mechanisms underlying hypoxia-induced neuronal apoptosis. Prog Neurobiol. 62:215-249. https://doi.org/10.1016/S0301-0082(00)00011-3
  7. Berridge KC. 2007. The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology (Berl) 191:391-431. https://doi.org/10.1007/s00213-006-0578-x
  8. Borta A, Hoglinger GU. 2007. Dopamine and adult neurogenesis. J Neurochem. 100:587-595. https://doi.org/10.1111/j.1471-4159.2006.04241.x
  9. Bromberg-Martin ES, Matsumoto M, Hikosaka O. 2010. Dopamine in motivational control: rewarding, aversive, and alerting. Neuron. 68:815-834. https://doi.org/10.1016/j.neuron.2010.11.022
  10. Chen WF, Chang H, Wong CS, Huang LT, Yang CH, Yang SN. 2007. Impaired expression of postsynaptic density proteins in the hippocampal CA1 region of rats following perinatal hypoxia. Exp Neurol. 204:400-410. https://doi.org/10.1016/j.expneurol.2006.12.002
  11. Fan LW, Lin S, Pang Y, Rhodes PG, Cai Z. 2006. Minocycline attenuates hypoxia-ischemia-induced neurological dysfunction and brain injury in the juvenile rat. Eur J Neurosci. 24:341-350. https://doi.org/10.1111/j.1460-9568.2006.04918.x
  12. Filippi A, Mahler J, Schweitzer J, Driever W. 2010. Expression of the paralogous tyrosine hydroxylase encoding genes th1 and th2 reveals the full complement of dopaminergic and noradrenergic neurons in zebrafish larval and juvenile brain. J Comp Neurol. 518:423-438. https://doi.org/10.1002/cne.22213
  13. Gage FH. 2002. Mini-review: neurogenesis in the adult brain. J Neurosci. 22:612-613.
  14. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. 1999. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci. 2:260-265 https://doi.org/10.1038/6365
  15. Grocott HP. 2009. Temperature regimens and neuroprotection during cardiopulmonary bypass: does rewarming rate matter? Anesth Analg. 109:1738-1740. https://doi.org/10.1213/ANE.0b013e3181bf246c
  16. Hachimi-Idrissi S, Van Hemelrijck A, Michotte A, Smolders I, Sarre S, Ebinger G, Huyghens L, Michotte Y. 2004. Postischemic mild hypothermia reduces neurotransmitter release and astroglial cell proliferation during reperfusion after asphyxial cardiac arrest in rats. Brain Res. 19: 217-225.
  17. Hurley FM, Costello DJ, Sullivan AM. 2004. Neuroprotective effects of delayed administration of growth/ differentiation factor-5 in the partial lesion model of Parkinson's disease. Exp Neurol. 185:281-289. https://doi.org/10.1016/j.expneurol.2003.10.003
  18. Jakowec MW, Nixon K, Hogg E, McNeill T, Petzinger GM. 2004. Tyrosine hydroxylase and dopamine transporter expression following 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine- induced neurodegeneration of the mouse nigrostriatal pathway. J Neurosci Res. 76:539-550. https://doi.org/10.1002/jnr.20114
  19. Kim YP, Kim H, Shin MS, Chang HK, Jang MH, Shin MC, Lee SJ, Lee HH, Yoon JH, Jeong IG, Kim CJ. 2004. Agedependence of the effect of treadmill exercise on cell proliferation in the dentate gyrus of rats. Neurosci Lett. 355:152-154. https://doi.org/10.1016/j.neulet.2003.11.005
  20. Kim DH, Ko IG, Kim BK, Kim TW, Kim SE, Shin MS, Kim CJ, Kim H, Kim KM, Baek SS. 2010a. Treadmill exercise inhibits traumatic brain injury-induced hippocampal apoptosis. Physiol Behav. 101:660-665 https://doi.org/10.1016/j.physbeh.2010.09.021
  21. Kim SE, Ko IG, Kim BK, Shin MS, Cho S, Kim CJ, Kim SH, Baek SS, Lee EK, Jee YS. 2010b. 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. https://doi.org/10.1016/j.exger.2010.02.005
  22. Kim SE, Ko IG, Kim BK, Sung YH, Shin MS, Cho S, Kim CJ, Kim KH, Lee KW, Kim DH. 2010c. Transplantation of human adipose-derived stem cells into the urethra ameliorates stress urinary incontinence and blunts the induction of c-Fos immunoreactivities in brain areas related to micturition in female rats. Anim Cells Syst. 14:237-244. https://doi.org/10.1080/19768354.2010.525839
  23. Ko IG, Shin MS, Kim BK, Kim SE, Sung YH, Kim TS, Shin MC, Cho HJ, Kim SC, Kim SH, Kim KH, Shin DH, Kim CJ. 2009. Tadalafil improves short-term memory by suppressing ischemia-induced apoptosis of hippocampal neuronal cells in gerbils. Pharmacol Biochem Behav. 91:629-635. https://doi.org/10.1016/j.pbb.2008.10.009
  24. Kobori N, Dash PK. 2006. Reversal of brain injury-induced prefrontal glutamic acid decarboxylase expression and working memory deficits by D1 receptor antagonism. J Neurosci. 26:4236-4246. https://doi.org/10.1523/JNEUROSCI.4687-05.2006
  25. Kumral E, Ozdemirkiran T, Alper Y. 2004. Strokes in the subinsular territory: clinical, topographical, and etiological patterns. Neurology. 28:2429-2432.
  26. Kvrivishvili G. 2002. Glycine and neuroprotective effect of hypothermia in hypoxic-ischemic brain damage. Neuroreport. 15:1995-2000.
  27. Lee KS, Lim BV, Jang MH, Shin MC, Lee TH, Kim YP, Shin HS, Cho SY, Kim H, Shin MS, Kim EH, Kim CJ. 2002. Hypothermia inhibits cell proliferation and nitric oxide synthase expression in rats. Neurosci Lett. 329:53-56. https://doi.org/10.1016/S0304-3940(02)00591-8
  28. Li C, Yan Z, Yang J, Chen H, Li H, Jiang Y, Zhang Z. 2010. Neuroprotective effects of resveratrol on ischemic injury mediated by modulating the release of neurotransmitter and neuromodulator in rats. Neurochem Int. 56:495-500 https://doi.org/10.1016/j.neuint.2009.12.009
  29. Liu J, Solway K, Messing RO, Sharp FR. 1998. Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci. 18:7768-78.
  30. Lledo PM, Alonso M, Grubb MS. 2006. Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci. 7:179-193. https://doi.org/10.1038/nrn1867
  31. Losiniecki A, Shutter L. 2010. Management of traumatic brain injury. Curr Treat Options Neurol. 12:142-154. https://doi.org/10.1007/s11940-010-0063-z
  32. Orset C, Parrot S, Sauvinet V, Cottet-Emard JM, Be'rod A, Pequignot JM, Denoroy L. 2005. Dopamine transporters are involved in the onset of hypoxia-induced dopamine efflux in striatum as revealed by in vivo microdialysis. Neurochem Int. 46:623-633. https://doi.org/10.1016/j.neuint.2005.02.005
  33. Park JH, Enikolopov G. 2010. Transient elevation of adult hippocampal neurogenesis after dopamine depletion. Exp Neurol. 222:267-276. https://doi.org/10.1016/j.expneurol.2010.01.004
  34. Parrot S, Cottet-Emard JM, Sauvinet V, Pequignot JM, Denoroy L. 2003. Effects of acute hypoxic conditions on extracellular excitatory amino acids and dopamine in the striatum of freely-moving rats. Adv Exp Med Biol. 536:433-444.
  35. Thoresen M, Hobbs CE, Wood T, Chakkarapani E, Dingley J. 2009. Cooling combined with immediate or delayed xenon inhalation provides equivalent long-term neuroprotection after neonatal hypoxia-ischemia. J Cereb Blood Flow Metab. 29:707-714. https://doi.org/10.1038/jcbfm.2008.163
  36. Vuckovic' MG, Wood RI, Holschneider DP, Abernathy A, Togasaki DM, Smith A, Petzinger GM, Jakowec MW. 2008. Memory, mood, dopamine, and serotonin in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned mouse model of basal ganglia injury. Neurobiol Dis. 32:319-327 https://doi.org/10.1016/j.nbd.2008.07.015
  37. Yanagisawa D, Qi M, Kim DH, Kitamura Y, Inden M, Tsuchiya D, Takata K, Taniguchi T, Yoshimoto K, Shimohama S, Akaike A, Sumi S, Inoue K. 2006. Improvement of focal ischemia-induced rat dopaminergic dysfunction by striatal transplantation of mouse embryonic stem cells. Neurosci Lett. 16:74-79.
  38. Zhao C, Deng W, Gage FH. 2008. Mechanisms and functional implications of adult neurogenesis. Cell. 132: 645-660. https://doi.org/10.1016/j.cell.2008.01.033

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