Difference in transient ischemia-induced neuronal damage and glucose transporter-1 immunoreactivity in the hippocampus between adult and young gerbils

Document Type : Original Article

Authors

1 Department of Emergency Medicine, School of Medicine, Kangwon National University, Chuncheon 200-701, South Korea

2 Department of Emergency Medicine, Sacred Heart Hospital, College of Medicine, Hallym University, Anyang431-796, South Korea

3 Department of Neurobiology, School of Medicine, Kangwon National University, Chuncheon 200-701, South Korea

4 Department of Physiology, College of Medicine, Hallym University, Chuncheon 200-702, South Korea

5 Department of Biomedical Science, Research Institute of Bioscience and Biotechnology, Hallym University, Chuncheon 200-702, South Korea

6 Department of Internal Medicine, School of Medicine, Kangwon National University, Chuncheon 200-701, South Korea

Abstract

Objective(s): The alteration of glucose transporters is closely related with the pathogenesis of brain edema. We compared neuronal damage/death in the hippocampus between adult and young gerbils following transient cerebral ischemia/reperfusion and changes of glucose transporter-1(GLUT-1)-immunoreactive microvessels in their ischemic hippocampal CA1 region.
Materials and Methods: Transient cerebral ischemia was developed by 5-min occlusion of both common carotid arteries. Neuronal damage was examined by cresyl violet staining, NeuN immunohistochemistry and Fluoro-Jade B histofluorescence staining and changes in GLUT-1 expression was carried out by immunohistochemistry.
Results: About 90% of pyramidal neurons only in the adult CA1 region were damaged after ischemia/reperfusion; in the young, about 53 % of pyramidal neurons were damaged from 7 days after ischemia/reperfusion. The density of GLUT-1-immunoreactive microvessels was significantly higher in the young sham-group than that in the adult sham-group. In the ischemia-operated-groups, the density of GLUT-1-immunoreactive microvessels was significantly decreased in the adult and young at 1 and 4 days post-ischemia, respectively, thereafter, the density of GLUT-1-immunoreactive microvessels was gradually increased in both groups after ischemia/reperfusion.
Conclusion: CA1 pyramidal neurons of the young gerbil were damaged much later than that in the adult and that GLUT-1-immunoreactive microvessels were significantly decreased later in the young. These data indicate that GLUT-1 might differently contribute to neuronal damage according to age after ischemic insults.

Keywords

References

1. George MG, Tong X, Kuklina EV, Labarthe DR. Trends in stroke hospitalizations and associated risk factors among children and young adults, 1995-2008. Ann Neurol 2011; 70:713-721.
2. Amlie-Lefond C, Sebire G, Fullerton HJ. Recent developments in childhood arterial ischaemic stroke. Lancet Neurol. 2008;7:425-35.
3. Lynch JK, Hirtz DG, DeVeber G, Nelson KB. Report of the National Institute of Neurological Disorders and Stroke workshop on perinatal and childhood stroke. Pediatrics 2002 ; 109:116-123.
4. Pan J, Konstas AA, Bateman B, Ortolano GA, Pile-Spellman J. Reperfusion injury following cerebral ischemia: pathophysiology, MR imaging, and potential therapies. Neuroradiology 2007; 49:93-102.
5. Eltzschig HK, Eckle T. Ischemia and reperfusion--from mechanism to translation. Nat Med 2011; 17:1391-1401.
6. Ogawa S, Gerlach H, Esposito C, Pasagian-Macaulay A, Brett J, Stern D. Hypoxia modulates the barrier and coagulant function of cultured bovine endothelium. Increased monolayer permeability and induction of procoagulant properties. J Clin Invest 1990; 85:1090-1998.
7. Zhao Y, Li Z, Wang R, Wei J, Li G, Zhao H. Angiopoietin 1 counteracts vascular endothelial growth factor-induced blood-brain barrier permeability and alleviates ischemic injury in the early stages of transient focal cerebral ischemia in rats. Neurol Res 2010; 32:748-755.
8. Hotchkiss RS, Strasser A, McDunn JE, Swanson PE. Cell death. N Engl J Med 2009 15; 361:1570-1583.
9. Oguro K, Miyawaki T, Yokota H, Kato K, Kamiya T, Katayama Y, et al. Upregulation of GluR2 decreases intracellular Ca2+ following ischemia in developing gerbils. Neurosci Lett 2004; 364:101-105.
10.  Kusumoto M, Arai H, Mori K, Sato K. Resistance to cerebral ischemia in developing gerbils. J Cereb Blood Flow Metab 1995; 15:886-891.
11. Seo JY, Yan BC, Park JH, Ahn JH, Kim IH, Lee JC, et al. Comparison of the immunoreactivities of NMDA receptors between the young and adult hippocampal CA1 region induced by experimentally transient cerebral ischemia. J Neurol Sci 2013; 325:108-114.
12. Yan BC, Park JH, Ahn JH, Choi JH, Yoo KY, Lee CH, et al. Comparison of glial activation in the hippocampal CA1 region between the young and adult gerbils after transient cerebral ischemia. Cell Mol Neurobiol 2012; 32:1127-1138.
13. Yan BC, Kim SK, Park JH, Ahn JH, Lee CH, Yoo KY, et al. Comparison of inflammatory cytokines changes in the hippocampal CA1 region between the young and adult gerbil after transient cerebral ischemia. Brain Res 2012; 1461:64-75.
14. Attwell D, Laughlin SB. An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 2001; 21:1133-1145.
15. Shestov AA, Emir UE, Kumar A, Henry PG, Seaquist ER, Oz G. Simultaneous measurement of glucose transport and utilization in the human brain. Am J Physiol Endocrinol Metab 2011; 301:E1040-1049.
16. Thorens B, Mueckler M. Glucose transporters in the 21st Century. Am J Physiol Endocrinol Metab 2010; 298:E141-145.
17. Simpson IA, Carruthers A, Vannucci SJ. Supply and demand in cerebral energy metabolism: the role of nutrient transporters. J Cereb Blood Flow Metab 2007; 27:1766-1791.
18. Farrell CL, Pardridge WM. Blood-brain barrier glucose transporter is asymmetrically distributed on brain capillary endothelial lumenal and ablumenal membranes: an electron microscopic immunogold study. Proc Natl Acad Sci U S A 1991; 88:5779-5783.
19. Gerhart DZ, LeVasseur RJ, Broderius MA, Drewes LR. Glucose transporter localization in brain using light and electron immunocytochemistry. J Neurosci Res 1989; 22:464-472.
20. Dwyer DS, Vannucci SJ, Simpson IA. Expression, regulation, and functional role of glucose transporters (GLUTs) in brain. Int Rev Neurobiol 2002; 51:159-188.
21. McCall AL, Van Bueren AM, Nipper V, Moholt-Siebert M, Downes H, Lessov N. Forebrain ischemia increases GLUT1 protein in brain microvessels and parenchyma. J Cereb Blood Flow Metab 1996; 16:69-76.
22. Urabe T, Hattori N, Nagamatsu S, Sawa H, Mizuno Y. Expression of glucose transporters in rat brain following transient focal ischemic injury. J Neurochem 1996; 67:265-271.
23. Lee CH, Park JH, Cho JH, Ahn JH, Yan BC, Lee JC, et al. Changes and expressions of Redd1 in neurons and glial cells in the gerbil hippocampus proper following transient global cerebral ischemia. J Neurol Sci 2014; 344:43-50.
24. Liu YR, Lei RY, Wang CE, Zhang BA, Lu H, Zhu HC, et al. Effects of catalpol on ATPase and amino acids in gerbils with cerebral ischemia/reperfusion injury. Neurol Sci 2014; 35:1229-1233.
25. Radenovic L, Selakovic V, Olivan S, Calvo AC, Rando A, Janac B, et al. Neuroprotective efficiency of tetanus toxin C fragment in model of global cerebral ischemia in Mongolian gerbils. Brain Res Bull 2014; 101:37-44.
26. Fukuchi T, Katayama Y, Kamiya T, McKee A, Kashiwagi F, Terashi A. The effect of duration of cerebral ischemia on brain pyruvate dehydrogenase activity, energy metabolites, and blood flow during reperfusion in gerbil brain. Brain Res 1998; 792:59-65.
27. Lorrio S, Negredo P, Roda JM, Garcia AG, Lopez MG. Effects of memantine and galantamine given separately or in association, on memory and hippocampal neuronal loss after transient global cerebral ischemia in gerbils. Brain Res 2009; 1254:128-137.
28. Kirino T, Sano K. Selective vulnerability in the gerbil hippocampus following transient ischemia. Acta Neuropathol 1984; 62:201-208.
29. Ohk TG, Yoo KY, Park SM, Shin BN, Kim IH, Park JH, et al. Neuronal damage using fluoro-jade B histofluorescence and gliosis in the striatum after various durations of transient cerebral ischemia in gerbils. Neurochem Res 2012; 37:826-834.
30. Burda J, Matiasova M, Gottlieb M, Danielisova V, Nemethova M, Garcia L, et al. Evidence for a role of second pathophysiological stress in prevention of delayed neuronal death in the hippocampal CA1 region. Neurochem Res 2005; 30:1397-1405.
31. Tamagaki C, Murata A, Asai S, Takase K, Gonno K, Sakata T, et al. Age-related changes of cornu ammonis 1 pyramidal neurons in gerbil transient ischemia. Neuropathology 2000; 20:221-227.
32. Lee CH, Yoo KY, Choi JH, Park OK, Hwang IK, Kim SK, et al. Neuronal damage is much delayed and microgliosis is more severe in the aged hippocampus induced by transient cerebral ischemia compared to the adult hippocampus. J Neurol Sci 2010; 294:1-6.
33. Crain BJ, Westerkam WD, Harrison AH, Nadler JV. Selective neuronal death after transient forebrain ischemia in the Mongolian gerbil: a silver impregnation study. Neuroscience 1988; 27:387-402.
34. Tortosa A, Ferrer I. Poor correlation between delayed neuronal death induced by transient forebrain ischemia, and immunoreactivity for parvalbumin and calbindin D-28k in developing gerbil hippocampus. Acta Neuropathol 1994; 88:67-74.
35. Yan BC, Park JH, Kim SK, Choi JH, Lee CH, Yoo KY, et al. Comparison of trophic factors changes in the hippocampal CA1 region between the young and adult gerbil induced by transient cerebral ischemia. Cell Mol Neurobiol 2012; 32:1231-1242.
36. Yan BC, Park JH, Ahn JH, Lee YJ, Lee TH, Lee CH, et al. Comparison of the immunoreactivity of Trx2/Prx3 redox system in the hippocampal CA1 region between the young and adult gerbil induced by transient cerebral ischemia. Neurochem Res 2012; 37:1019-1030.
37. Yan BC, Park JH, Lee CH, Yoo KY, Choi JH, Lee YJ, et al. Increases of antioxidants are related to more delayed neuronal death in the hippocampal CA1 region of the young gerbil induced by transient cerebral ischemia. Brain Res 2011; 1425:142-154.
38. Jorgensen MB, Wright DC, Diemer NH. Postischemic glucose metabolism is modified in the hippocampal CA1 region depleted of excitatory input
or pyramidal cells. J Cereb Blood Flow Metab 1990; 10:243-251.
39. Leybaert L. Neurobarrier coupling in the brain: a partner of neurovascular and neurometabolic coupling? J Cereb Blood Flow Metab 2005; 25:2-16.
40. Gerhart DZ, Leino RL, Taylor WE, Borson ND, Drewes LR. GLUT1 and GLUT3 gene expression in gerbil brain following brief ischemia: an in situ hybridization study. Brain Res Mol Brain Res 1994; 25:313-322.
41. Lee WH, Bondy CA. Ischemic injury induces brain glucose transporter gene expression. Endocrinology 1993; 133:2540-2544.
42. Lawrence MS, Sun GH, Kunis DM, Saydam TC, Dash R, Ho DY, et al. Overexpression of the glucose transporter gene with a herpes simplex viral vector protects striatal neurons against stroke. J Cereb Blood Flow Metab 1996; 16:181-185.
43. Zhang WW, Zhang L, Hou WK, Xu YX, Xu H, Lou FC, et al. Dynamic expression of glucose transporters 1 and 3 in the brain of diabetic rats with cerebral ischemia reperfusion. Chin Med J (Engl) 2009; 122:1996-2001.
44. Li X, Han H, Hou R, Wei L, Wang G, Li C, et al. Progesterone treatment before experimental hypoxia-ischemia enhances the expression of glucose transporter proteins GLUT1 and GLUT3 in neonatal rats. Neurosci Bull 2013; 29:287-294.
45. Vannucci SJ, Seaman LB, Vannucci RC. Effects of hypoxia-ischemia on GLUT1 and GLUT3 glucose transporters in immature rat brain. J Cereb Blood Flow Metab 1996; 16:77-81.
46. Vannucci SJ, Reinhart R, Maher F, Bondy CA, Lee WH, Vannucci RC, et al. Alterations in GLUT1 and GLUT3 glucose transporter gene expression following unilateral hypoxia-ischemia in the immature rat brain. Brain Res Dev Brain Res 1998; 107:255-264.
47. Harik SI, Behmand RA, LaManna JC. Hypoxia increases glucose transport at blood-brain barrier in rats. J Appl Physiol (1985) 1994; 77:896-901.
48. Loike JD, Cao L, Brett J, Ogawa S, Silverstein SC, Stern D. Hypoxia induces glucose transporter expression in endothelial cells. Am J Physiol 1992; 263:C326-333.
49. Abdul Muneer PM, Alikunju S, Szlachetka AM, Murrin LC, Haorah J. Impairment of brain endothelial glucose transporter by methamphetamine causes blood-brain barrier dysfunction. Mol Neurodegener 2011; 6:23.
 
Iranian Journal of Basic Medical Sciences
Volume 19, Issue 5
May 2016
Pages 521-528

Files

Share

How to cite

Statistics