Exercise pre-conditioning ameliorates blood-brain barrier dysfunction in stroke by enhancing basal lamina

Neurological Research

Volumn 29, Issue 4, 2007, Pages 382-387

  Davis, William ^a   Mahale, Seema ^a   Carranza, Aaron ^a   Cox, Brian ^a   Hayes, Katie ^a   Jimenez, David ^a   Ding, Yuchuan ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Collagen IV; ECM; Ex vivo; Ischemia and reperfusion injury; MMP 9

Indexed keywords

COLLAGEN TYPE 4; GELATINASE B;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CORTEX; BRAIN EDEMA; CAPILLARY BASEMENT MEMBRANE; CAPILLARY PERMEABILITY; COLLAGEN SYNTHESIS; CONTROLLED STUDY; CORPUS STRIATUM; EXERCISE; IMMUNOCYTOCHEMISTRY; MALE; NONHUMAN; RAT; REPERFUSION INJURY; STEREOLOGY; STROKE; WESTERN BLOTTING;

ANIMALS; BASEMENT MEMBRANE; BEHAVIOR, ANIMAL; BLOOD-BRAIN BARRIER; BRAIN; BRAIN EDEMA; CEREBROVASCULAR ACCIDENT; COLLAGEN TYPE IV; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; MALE; MATRIX METALLOPROTEINASE 9; NEOVASCULARIZATION, PATHOLOGIC; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY;

EID: 34547576745     PISSN: 01616412     EISSN: None     Source Type: Journal    
DOI: 10.1179/016164107X204701     Document Type: Article

References (55)

1. Stummer W, Weber K, Tranmer B, et al. Reduced mortality and brain damage after locomotor activity in gerbil forebrain ischemia. Stroke 1994; 25: 1862-1869
2. Stummer W, Baethmann A, Murr R, et al. Cerebral protection against ischemia by locomotor activity in gerbils. Underlying mechanisms. Stroke 1995; 26: 1423-1429
3. Wang RY, Yang YR, Yu SM. Protective effects of treadmill training on infarction in rats. Brain Res 2001; 922: 140-143
4. Ang ET, Wong PT, Moochhala S, et al. Neuroprotection associated with running: Is it a result of increased endogenous neurotrophic factors? Neuroscience 2003; 118: 335-345
5. Ding Y, Li J, Luan X, et al. Exercise pre-conditioning reduces brain damage in ischemic rats that may be associated with regional angiogenesis and cellular overexpression of neurotrophin. Neuroscience 2004; 124; 583-591
6. Li J, Luan X, Clark J, et al. Neuroprotection against transient cerebral ischemia by exercise pre-conditioning in rats. Neurol Res 2004; 26: 404-408
7. Ding Y, Li J, Rafols JA, et al. Pre-ischemic motor exercise reduces ischemia/reperfusion injury in rats that correlateds with regional angiogenesis and cellular expression of neurotrophin. Stroke 2003; 34: 240-241
8. Endres M, Gertz K, Lindauer U, et al. Mechanisms of stroke protection by physical activity. Ann Neurol 2003; 54: 582-590
9. Ding YH, Young CN, Luan X, et al. Exercise preconditioning ameliorates inflammatory injury in ischemic rats during reperfusion. Acta Neuropathol (Berl) 2005; 3: 237-246
10. Ding YH, Luan X, Li J, et al. Exercise-induced overexpression of angiogenic factors and reduction of ischemia/reperfusion injury in stroke. Curr Neurovasc Res 2004; 1: 411-420
11. Ding Y, Ding YH, Li J, et al. Exercise induces integrin overexpression and improves neurovascular integrity in ischemic stroke. Stroke 2005; 36: 470
12. Ding YH, Ding Y, Li J, et al. Exercise pre-conditioning strengthens brain microvascular integrity in a rat stroke model. Neurol Res 2006; 28: 184-189
13. del Zoppo GJ, Mabuchi T. Cerebral microvessel responses to focal ischemia. J Cereb Blood Flow Metab 2003; 23: 879-894
14. Ayata C, Ropper AH. Ischaemic brain oedema. J Clin Neurosci 2002; 9: 113-124
15. Neuwelt CM. The role of plasmapheresis in the treatment of severe central nervous system neuropsychiatric systemic lupus erythematosus. Ther Apher Dial 2003; 7: 173-182
16. Yang GY, Betz AL. Reperfusion-induced injury to the blood-brain barrier after middle cerebral artery occlusion in rats. Stroke 1994; 25: 1658-1664
17. Hamann GF, Okada Y, Fitridge R, et al. Microvascular basal lamina antigens disappear during cerebral ischemia and reperfusion. Stroke 1995; 26: 2120-2126
18. Lo EH, Dalkara T, Moskowitz MA. Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 2003; 4: 399-415
19. Gasche Y, Fujimura M, Morita F, et al. Early appearance of activated matrix metalloproteinase-9 after focal cerebral ischemia in mice: A possible role in blood-brain barrier dysfunction. J Cereb Blood Flow Metab 1999; 19: 1020-1028
20. Fujimura M, Gasche Y, Morita F, et al. Early appearance of activated matrix metalloproteinase-9 and blood-brain barrier disruption in mice after focal cerebral ischemia and reperfusion. Brain Res 1999; 842: 92-100
21. Rosenberg CA, Estrada EY, Dencoff JE. Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke 1998; 29: 2189-2195
22. Heo JH, Lucero J, Abumiya T, et al. Matrix metalloproteinases increase very early during experimental focal cerebral ischemia. J Cereb Blood Flow Metab 1999; 19: 624-633
23. Wagner S, Nagel S, Kluge B, et al. Topographically graded postischemic presence of metalloproteinases is inhibited by hypothermia. Brain Res 2003; 984: 63-75
24. Ding Y, Li J, Clark J, et al. Synaptic plasticity in thalamic nuclei enhanced by motor skill training in rat with transient middle cerebral artery occlusion. Neurol Res 2003; 25: 189-194
25. Ding Y, Li J, Lai Q, et al. Functional improvement after motor training is correlated with synaptic plasticity in rat thalamus. Neurol Res 2002; 24: 829-836
26. Li J, Ding YH, Rafols JA, et al. Increased astrocyte proliferation in rats after running exercise. Neurosci Lett 2005; 3: 160-164
27. Zea Longa Z, Weinstein PR, Carlson S, et al. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 1989; 20: 84-91
28. Belayev L, Alonso OF, Busto R, et al. Middle cerebral artery occlusion in the rat by intraluminal suture. Neurological and pathological evaluation of an improved model. Stroke 1996; 27: 1616-1622
29. Masada T, Hua Y, Xi G, et al. Attenuation of ischemic brain edema and cerebrovascular injury after ischemic preconditioning in the rat. J Cereb Blood Flow Metab 2001; 21: 22-33
30. Kawai N, Kawanishi M, Okauchi M, et al. Effects of hypothermia on thrombin-induced brain edema formation. Brain Res 2001; 895: 50-58
31. Ding YC, Azam S, DeGracia DJ, et al. Focal brain ischemia and reperfusion associated with modifications in eukaryotic initiation factor 2-a. Stroke 2002; 33: 400-401
32. Lindsey ML, Goshorn DK, Squires CE, et al. Age-dependent changes in myocardial matrix metalloproteinase/tissue inhibitor of metalloproteinase profiles and fibroblast function. Cardiovasc Res 2005; 66: 410-419
33. Fukuda S, Fini CA, Mabuchi T, et al. Focal cerebral ischemia induces active proteases that degrade microvascular matrix. Stroke 2004; 35: 998-1004
34. Gundersen HJ, Bendtsen TF, Korbo L, et al. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 1988; 96: 379-394
35. Kleim JA, Cooper NR, VandenBerg PM. Exercise induces angiogenesis but does not alter movement representations within rat motor cortex. Brain Res 2002; 934: 1-6
36. Swain RA, Harris AB, Wiener EC, et al. Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 2003; 117: 1037-1046
37. Betz AL, Dietrich WD. Blood-brain barrier dysfunction in cerebral ischemia. In: Ginsberg MD, Bogousslavsky J, eds. Cerebrovascular Disease Pathophysiology, Diagnosis, and Management, Malden, MA: Blackwell Science, 1998: pp. 358-370
38. Wang X, Lo EH. Triggers and mediators of hemorrhagic transformation in cerebral ischemia. Mol Neurobiol 2003; 28: 229-244
39. Petty MA, Lo EH. Junctional complexes of the blood-brain barrier: Permeability changes in neuroinflammation. Prog Neurobiol 2002; 68: 311-323
40. Petty MA, Wettstein JG. Elements of cerebral microvascular ischaemia. Brain Res Brain Res Rev 2001; 36: 23-34
41. Robertson PL, Du B, Bowman PD, et al. Angiogenesis in developing rat brain: An in vivo and in vitro study. Brain Res 1985; 355: 219-223
42. Ogunshola OO, Stewart WB, Mihalcik V, et al. Neuronal VEGF expression correlates with angiogenesis in postnatal developing rat brain. Brain Res Dev Brain Res 2000; 119: 139-153
43. Black JE, Isaacs KR, Anderson BJ, et al. Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc Natl Acad Sci USA 1990; 87: 5568-5572
44. Isaacs KR, Anderson BJ, Alcantara AA, et al. Exercise and the brain: angiogenesis in the adult rat cerebellum after vigorous physical activity and motor skill learning. J Cereb Blood Flow Metab 1992; 12: 110-119
45. Ding Y, Ding YH, Luan X, et al. Neuroprotective effect of exercise-induced angiogenic factors on ischemia/reperfusion injury in stroke. Stroke 2004; 35: 273
46. Vissing J, Andersen M, Diemer NH. Exercise-induced changes in local cerebral glucose utilization in the rat. J Cereb Blood Flow Metab 1996; 16: 729-736
47. Romanic AM, White RF, Arleth AJ, et al. Matrix metalloproteinase expression increases after cerebral focal ischemia in rats: Inhibition of matrix metalloproteinase-9 reduces infarct size. Stroke 1998; 29: 1020-1030
48. Planas AM, Sole S, Justicia C. Expression and activation of matrix metalloproteinase-2 and -9 in rat brain after transient focal cerebral ischemia. Neurobiol Dis 2001; 8: 834-846
49. Planas AM, Sole S, Justicia C, et al. Estimation of gelatinase content in rat brain: Effect of focal ischemia. Biochem Biophys Res Commun 2000; 278: 803-807
50. Pfefferkorn T, Rosenberg GA. Closure of the blood-brain barrier by matrix metalloproteinase inhibition reduces rtPA-mediated mortality in cerebral ischemia with delayed reperfusion. Stroke 2003; 34: 2025-2030
51. Clark AW, Krekoski CA, Bou SS, et al. Increased gelatinase A (MMP-2) and gelatinase B (MMP-9) activities in human brain after focal ischemia. Neurosci Lett 1997; 238: 53-56
52. Horstmann S, Kalb P, Koziol J, et al. Profiles of matrix metalloproteinases, their inhibitors, and laminin in stroke patients: Influence of different therapies. Stroke 2003; 34: 2165-2170
53. Asahi M, Wang X, Mori T, et al. Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J Neurosci 2001; 21: 7724-7732
54. Asahi M, Asahi K, Jung JC, et al. Role for matrix metalloproteinase 9 after focal cerebral ischemia: Effects of gene knockout and enzyme inhibition with BB-94. J Cereb Blood Flow Metab 2000; 20: 1681-1689
55. Wang X, Jung J, Asahi M, et al. Effects of matrix metalloproteinase-9 gene knock-out on morphological and motor outcomes after traumatic brain injury. J Neurosci 2000; 20: 7037-7042