Chronic brain hypoperfusion causes early glial activation and neuronal death, and subsequent long-term memory impairment

Brain Research Bulletin

Volumn 87, Issue 1, 2012, Pages 109-116

  Cechetti, Fernanda ^a   Pagnussat, Aline S ^b   Worm, Paulo V ^a   Elsner, Viviane Rostirolla ^a   Ben, Juliana ^a   da Costa, Marcelo Siveira ^a   Mestriner, Régis ^a   Weis, Simone Nardin ^a   Netto, Carlos Alexandre ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b UNIVERSIDADE FEDERAL DE CIÊNCIAS DA SAÚDE DE PORTO ALEGRE   (Brazil)

Author keywords

2VO ischemia memory impairment; Chronic cerebral hypoperfusion; Glia; Hippocampus; Memory impairment; Neuron

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; NEURON SPECIFIC NUCLEAR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; BRAIN BLOOD FLOW; BRAIN DYSFUNCTION; BRAIN ISCHEMIA; BRAIN PERFUSION; BRAIN SIZE; CELL DAMAGE; CELL LOSS; COGNITIVE DEFECT; COMMON CAROTID ARTERY; CONTROLLED STUDY; DEMENTIA; GLIA; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; IMMUNOREACTIVITY; LONG TERM MEMORY; MALE; MEMORY DISORDER; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL MEMORY; TASK PERFORMANCE; WORKING MEMORY;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CELL DEATH; MALE; MAZE LEARNING; MEMORY DISORDERS; MEMORY, LONG-TERM; NEUROGLIA; NEURONS; RATS; RATS, WISTAR;

EID: 84155172587     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2011.10.006     Document Type: Article

References (53)

1. De la Torre J.C. Impaired brain microcirculation may trigger Alzheimer's disease. Neurosci. Biobehav. Rev. 1994, 18:397-401.
2. Ohta H., Nishikawa H., Kimura H., Anayama H., Miyamoto M. Chronic cerebral hypoperfusion by permanent internal carotid ligation produces learning impairment without brain damage in rats. Neurosc. 1997, 79:1039-1050.
3. Komatani A., Yamaguchi K., Sugai Y., Takanashi T., Kera M., Shinohara M., Kawakatsu S. Assessment of demented patients by dynamic SPECT of inhaled xenon-133. J. Nucl. Med. 1988, 29:1621-1626.
4. Ni J.W., Ohta H., Matsumoto K., Watanabe H. Progressive cognitive impairment following chronic cerebral hypoperfusion induced by permanent occlusion of bilateral carotid arteries in rats. Brain Res. 1994, 653:231-236.
5. Farkas E., Luiten P.G.M., Baric F. Permanent, bilateral common carotid artery occlusion in the rat: A model for chronic cerebral hypoperfusion-related neurodegenerative diseases. Brain Res. Reviews 2007, 54:162-180.
6. Otori T., Katsumata T., Muramatsu H., Kashiwagi F., Katayama Y., Terashi A. Long-term measurements of cerebral blood flow and metabolism in a rat chronic hypoperfusion model. Clin. Exp. Pharmacol. Physiol. 2003, 30:266-272.
7. Tsuchiya M., Sako K., Yura S., Yonemasu Y. Cerebral blood flow and histopathological changes following permanent bilateral carotid artery ligation in Wistar rats. Exp. Brain Res. 1992, 89:87-92.
8. Ulrich P.T., Kroppenstedt S., Heimann A., Kempski O. Laser-Doppler scanning of local cerebral blood flow and reserve capacity and testing of motor and memory functions in a chronic 2-vessel occlusion model in rats. Stroke 1998, 29:2412-2420.
9. Pappas B.A., De la Torre J.C., Davidson C.M., Keyes M.T., Fortin T. Chronic reduction of cerebral blood flow in the adult rat: late-emerging CA1 cell loss and memory dysfunction. Brain Res. 1996, 708:50-58.
10. Sarti C., Pantoni L., Bartolini L., Inzitari D. Cognitive impairment and chronic cerebral hypoperfusion: what can be learned from experimental models. J. Neurol. Sci. 2002, 204:263-266.
11. Bennett S.A., Tenniswood M., Chen J.H., Davidson C.M., Keyes M.T., Fortin T., Pappas B.A. Chronic cerebral hypoperfusion elicits neuronal apoptosis and behavioral impairment. Neuroreport 1998, 9:161-166.
12. Farkas E., Donka G., de Vos R.A.I., Mihaly A., Bari F., Luiten P.G.M. Experimental cerebral hypoperfusion induces white matter injury and microglial activation in the rat brain. Acta Neuropathol. 2004, 108:57-64.
13. Farkas E., Timmer N.M., Domoki F., Mihály A., Luiten P.G., Bari F. Ischemic administration of diazoxide attenuates long-term microglial activation in the rat brain after permanent carotid artery occlusion. Neurosci. Lett. 2005, 387:168-172.
14. Institoris A., Farkas E., Berczi S., Sule Z., Bari F. Effects of cyclooxygenase (COX) inhibition on memory impairment and hippocampal damage in the early period of cerebral hypoperfusion in rats. Eur. J. Pharmacol. 2007, 574:29-38.
15. Cechetti F., Worm P.V., Pereira L.O., Siqueira I.R., Netto C.A. The modified 2VO ischemia protocol causes similar cognitive impairment with better survival rate, as compared to standard method. Braz. J. Med. Biol. Res. 2010, 43:1178-1183.
16. Maragakis N.J., Rothstein J.D. Glutamate transporters: animal models to neurologic disease. Neurobiol. Dis. 2004, 15:461-473.
17. Vicente E., Degerone D., Bohn L., Scornavaca F., Pimentel A., Leite M.C., Swarowsky A., Rodrigues L., Nardin P., Almeida L.M.V., Gottfried C., Souza D.O., Netto C.A., Gonçalves C.A. Astroglial and cognitive effects of chronic cerebral hypoperfusion in the rat. Brain Res. 2009, 1251:204-212.
18. Eng L.F., Ghirnikar R.S., Lee Y.L. Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochem. Res. 2000, 25:1439-1451.
19. Vicente E., Bôer M., Leite M., Silva M., Tramontina F., Porciúncula L., Dalmaz C., Gonçalves C.A. Cerebrospinal fluid S100B increases reversibly in neonates of methyl mercury-intoxicated pregnant rats. Neurotoxicology 2004, 25:771-777.
20. Liu H.X., Zhang J.J., Zheng P., Zhang Y. Altered expression of MAP-2, GAP-43, and synaptophysin in the hippocampus of rats with chronic cerebral hypoperfusion correlates with cognitive impairment. Brain Res. Mol. Brain Res. 2005, 139:169-177.
21. Farkas E., Institóris A., Domoki F., Mihály A., Bari F. The effect of pre- and posttreatment with diazoxide on the early phase of chronic cerebral hypoperfusion in the rat. Brain Res. 2004, 1087:168-174.
22. Sarti C., Pantoni L., Bartolini L., Inzitari D. Persistent impairment of gait performances and working memory after bilateral common carotid artery occlusion in the adult Wistar rat. Behav. Brain Res. 2002, 136:13-20.
23. Lavinsky D., Arterni N.S., Achaval M., Netto C.A. Chronic bilateral common carotid artery occlusion: a model for ocular ischemic syndrome in the rat. Graefe Arch. Clin. Exp. Ophthalmol. 2006, 244:199-204.
24. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 1984, 11:47-60.
25. Netto C.A., Hodges H., Sinden J.D., Le Peillet E., Kershaw T., Sowinski P., et al. Effects of fetal hippocampal grafts on ischaemic-induced deficits in spatial navigation in the water maze. Neurosc. 1993, 54:69-92.
26. Pereira L.O., Strapasson A.C., Nabinger P.M., Achaval M., Netto C.A. Early enriched housing results in partial recovery of memory deficits in female, but not in male, rats after neonatal hypoxia-ischemia. Brain Res. 2007, 1218:257-266.
27. Bevins R.A., Besheer J. Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study 'recognition memory'. Nature Protocols 2006, 1:1306-1311.
28. Plamondon H., Morin A., Charron C. Chronic 17beta-estradiol pretreatment and ischemia-induced hippocampal degeneration and memory impairments: a 6-month survival study. Horm. Behav. 2006, 50:361-369.
29. Botton P.H., Costa M.S., Ardais A.P., Mioranzza S., Souza D.O., da Rocha J.B., Porciúncula L.O. Caffeine prevents disruption of memory consolidation in the inhibitory avoidance and novel object recognition tasks by scopolamine in adult mice. Behav. Brain Res. 2010, 214:254-259.
30. Costa M.S., Botton P.H., Mioranzza S., Ardais A.P., Moreira J.D., Souza D.O., Porciúncula L.O. Caffeine improves adult mice performance in the object recognition task and increases BDNF and TrkB independent of phospho-CREB immunocontent in the hippocampus. Neurochem. Int. 2008, 53:89-94.
31. Netto C.A., Dias R.D., Izquierdo I. Differential effect of posttraining naloxone, beta-endorphin, leu-enkephalin and electroconvulsive shock administration upon memory of an open-field habituation and of a water-finding task. Psychoneuroendocrinology 1986, 11:437-446.
32. Lavinsky D., Arteni N.S., Netto C.A. Agmatine induces anxiolysis in the elevated plus maze task in adult rats. Behav. Brain Res. 2003, 141:19-24.
33. Miki T., Satriotomo I., Li H., Matsumoto Y., Gu H., Yokoyama T., et al. Application of the physical disector to the central nervous system: estimation of the total number of neurons in subdivisions of the rat hippocampus. Anatomical Sci. Int. 2005, 80:153-162.
34. Rodrigues A.L., Harten N.S., Abel C., Zylbersztejn D., Chazan R., Viola G., et al. Tactile stimulation and maternal separation prevent hippocampal damage in rats submitted to neonatal hypoxiaischemia. Brain Res. 2004, 1002:94-99.
35. Pereira L.O., Arteni N.S., Petersen R.C., da Rocha A.P., Achaval M., Netto C.A. Effects of daily environmental enrichment on memory deficits and brain injury following neonatal hypoxia-ischemia in the rat. Neurobiol. Learn. Mem. 2007, 87:101-108.
36. Schmidt-Karsten R., Aguirre-Chen C., Saul I., Yick L., Hamasaki D., Busto R., Ginsberg M.D. Astrocytes react to oligemia in the forebrain induced by chronic bilateral common carotid artery occlusion in rats. Brain Res. 2005, 1052:28-39.
37. Zhao Q., Murakami Y., Tohda M., Watanabe H., Matsumoto K. Preventive effect of chotosan, a Kampo medicine, on transient ischemia-induced learning deficit is mediated by stimulation of muscarinic M1 but not nicotinic receptor. Biol. Pharm. Bull. 2005, 28:1873-1878.
38. Kim D.H., Jin Jeon S., Son S.H., Jung J.W., Lee S., Hoon Yoon B., Choi J.W., Cheong J.H., Ko K.H., Ryu J.H. Effect of the flavonoid, oroxylin A, on transient cerebral hypoperfusion induced memory impairment in mice. Pharmacol. Biochem. Behav. 2006, 85:658-668.
39. De Bortoli V.C., Zangrossi J.H., De Guiar, Almeida S.S., De Oliveira A.M. Inhibitory avoidance memory retention in the elevated T-maze is impaired after perivascular manipulation of the common carotid arteries. Life Sci. 2005, 18:2103-2114.
40. Choy M., Ganesan V., Thomas D.L., Thornton J.S., Proctor E., King M.D., van der Weerd L., Gadian D.G., Lythgoe M.F.J. The chronic vascular and haemodynamic response after permanent bilateral common carotid occlusion in newborn and adult rats. Cereb. Blood. Flow. Metab. 2006, 26:1066-1075.
41. Oldendorf W.H. Trophic changes in the arteries at the base of the rat brain in response to bilateral common carotid ligation. J. Neuropathol. Exp. Neurol. 1989, 48:534-547.
42. De Jong G.I., Farkas E., Plass J., Keijser J.N., de la Torre J.C., Luiten P.G.M. Cerebral hypoperfusion yields capillary damage in hippocampus CA1 that correlates to spatial memory impairment. Neurosc. 1999, 91:203-210.
43. Logothetis N.K., Sheinberg D.L. Visual object recognition. Annu. Rev. Neurosci. 1996, 19:577-621.
44. Riesenhuber M., Poggio T. Neural mechanisms of object recognition. Curr. Opin. Neurobiol. 2002, 12:162-168.
45. Nunn J.A., Hodges H. Cognitive deficits induced by global cerebral ischaemia: relationship to brain damage and reversal by transplants. Behav. Brain Res. 1994, 65:1-31.
46. Xiong Z., Liu C., Wang F., Li C., Wang W., Wang J., et al. Protective effects of breviscapine on ischemic vascular dementia in rats. Biol. Pharm. Bull. 2006, 29:1880-1885.
47. De Butte M., Fortin T., Pappas B.A. Pinealectomy: behavioral and neuropathological consequences in a chronic cerebral hypoperfusion model. Neurobiol. Aging. 2002, 23:309-317.
48. Plaschke K., Grant M., Weigand M.A., Zuchner J., Martin E., Bardenheuer H.J. Neuromodulatory effect of propentofylline on rat brain under acute and long-term hypoperfusion. Br. J. Pharmacol. 2001, 133:107-116.
49. Murakami Y., Zhao Q., Harada K., Tohda M., Watanabe H., Matsumoto K. Chotosan, a Kampo formula, improves chronic cerebral hypoperfusion-induced spatial learning deficit via stimulation of muscarinic M1 receptor. Pharmacol. Biochem. Behav. 2005, 81:616-625.
50. O'Callaghan J.P., Sriram K. Glial fibrillary acidic protein and related glial proteins as biomarkers of neurotoxicity. Expert. Opin. Drug Saf. 2005, 4:433-442.
51. Beck H., Plate K.H. Angiogenesis after cerebral ischemia. Acta Neuropathol. 2009, 117:481-496.
52. Thiel G. Synapsin I, synapsin II, and synaptophysin: marker proteins of synaptic vesicles. Brain Pathol. 1993, 3:87-95.
53. Zhu H., Zhang J., Sun H., Zhang L., Liu H., Zeng X., Yang Y., Yao Z. An enriched environment reverses the synaptic plasticity deficit induced by chronic cerebral hypoperfusion. Neurosci. Lett. 2011, 502:71-75.