Ultrastructural analysis of blood-brain barrier breakdown in the peri-infarct zone in young adult and aged mice

Journal of Cerebral Blood Flow and Metabolism

Volumn 36, Issue 2, 2016, Pages 413-425

  Nahirney, Patrick C ^a,b   Reeson, Patrick ^a   Brown, Craig E ^a,b  

^a UNIVERSITY OF VICTORIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

aging; astrocytes; basement membrane; blood brain barrier; endothelium; extravasation; ischemia; pericytes; Stroke; transcytosis

Indexed keywords

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BASEMENT MEMBRANE; BLOOD BRAIN BARRIER; BRAIN INFARCTION; BRAIN ISCHEMIA; BRAIN MITOCHONDRION; BRAIN PERICYTE; CAVEOLA; CELL VACUOLE; CONTROLLED STUDY; ENDOTHELIUM CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TIGHT JUNCTION; ULTRASTRUCTURE; YOUNG ADULT; AGING; ANIMAL; C57BL MOUSE; CEREBROVASCULAR ACCIDENT; MITOCHONDRION; MITOCHONDRION SWELLING; OCCLUSIVE CEREBROVASCULAR DISEASE; PATHOLOGY; PERICYTE; PERMEABILITY; VASCULAR ENDOTHELIUM;

AGING; ANIMALS; ASTROCYTES; BASEMENT MEMBRANE; BLOOD-BRAIN BARRIER; BRAIN ISCHEMIA; CAVEOLAE; CEREBRAL INFARCTION; ENDOTHELIUM, VASCULAR; INTRACRANIAL THROMBOSIS; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL SWELLING; PERICYTES; PERMEABILITY; STROKE; TIGHT JUNCTIONS; VACUOLES;

EID: 84961289369     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1177/0271678X15608396     Document Type: Article

References (41)

1. Ballabh P, Braun A and Nedergaard M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol Dis 2004; 16: 1-13.
2. Hawkins BT and Davis TP. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 2005; 57: 173-185.
3. Reeson P, Tennant KA, Gerrow K, et al. Delayed inhibition of VEGF signaling after stroke attenuates bloodbrain barrier breakdown and improves functional recovery in a comorbidity-Dependent manner. J Neurosci 2015; 35: 5128-5143.
4. del Zoppo GJ and Mabuchi T. Cerebral microvessel responses to focal ischemia. J Cereb Blood Flow Metab 2003; 23: 879-894.
5. Chen B, Friedman B, Cheng Q, et al. Severe blood-brain barrier disruption and surrounding tissue injury. Stroke 2009; 40: e666-E674.
6. Tomkins O, Friedman O, Ivens S, et al. Blood-brain barrier disruption results in delayed functional and structural alterations in the rat neocortex. Neurobiol Dis 2007; 25: 367-377.
7. Shinnou M, Ueno M, Sakamoto H, et al. Blood-brain barrier damage in reperfusion following ischemia in the hippocampus of the Mongolian gerbil brain. Acta Neurol Scand 1998; 98: 406-411.
8. Bell RD, Winkler EA, Sagare AP, et al. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 2010; 68: 409-427.
9. Fernandez-Lopez D, Faustino J, Daneman R, et al. Blood-brain barrier permeability is increased after acute adult stroke but not neonatal stroke in the rat. J Neurosci 2012; 32: 9588-9600.
10. Knowland D, Arac A, Sekiguchi KJ, et al. Stepwise recruitment of transcellular and paracellular pathways underlies blood-brain barrier breakdown in stroke. Neuron 2014; 82: 603-617.
11. Bolton SJ, Anthony DC and Perry VH. Loss of the tight junction proteins occludin and zonula occludens-1 from cerebral vascular endothelium during neutrophil-induced blood-brain barrier breakdown in vivo. Neuroscience 1998; 86: 1245-1257.
12. Krueger M, Hartig W, Reichenbach A, et al. Blood-brain barrier breakdown after embolic stroke in rats occurs without ultrastructural evidence for disrupting tight junctions. PLoS One 2013; 8: e56419.
13. Westergaard E, Go G, Klatzo I, et al. Increased permeability of cerebral vessels to horseradish peroxidase induced by ischemia in Mongolian Gerbils. Acta Neuropathol 1976; 35: 307-325.
14. Lossinsky AS and Shivers RR. Structural pathways for macromolecular and cellular transport across the bloodbrain barrier during inflammatory conditions. Histol Histopathol 2004; 19: 535-564.
15. Dietrich WD, Busto R, Halley M, et al. The importance of brain temperature in alterations of the blood-brain barrier following cerebral ischemia. J Neuropathol Exp Neurol 1990; 49: 486-497.
16. Jackman K, Kahles T, Lane D, et al. Progranulin deficiency promotes post-ischemic blood-brain barrier disruption. J Neurosci 2013; 33: 19579-19589.
17. Sagare AP, Bell RD, Zhao Z, et al. Pericyte loss influences Alzheimer-like neurodegeneration in mice. Nat Commun 2013; 4: 2932.
18. Armulik A, Genove G, Mae M, et al. Pericytes regulate the blood-brain barrier. Nature 2010; 468: 557-561.
19. Ito U, Hakamata Y, Kawakami E, et al. Temporary [corrected] cerebral ischemia results in swollen astrocytic end-feet that compress microvessels and lead to delayed [corrected] focal cortical infarction. J Cereb Blood Flow Metab 2011; 31: 328-338.
20. Risher WC, Croom D and Kirov SA. Persistent astroglial swelling accompanies rapid reversible dendritic injury during stroke-induced spreading depolarizations. Glia 2012; 60: 1709-1720.
21. Kwon I, Kim EH, del Zoppo GJ, et al. Ultrastructural and temporal changes of the microvascular basement membrane and astrocyte interface following focal cerebral ischemia. J Neurosci Res 2009; 87: 668-676.
22. Ueno M, Tomimoto H, Akiguchi I, et al. Blood-brain barrier disruption in white matter lesions in a rat model of chronic cerebral hypoperfusion. J Cereb Blood Flow Metab 2002; 22: 97-104.
23. Mooradian AD. Effect of aging on the blood-brain barrier. Neurobiol Aging 1988; 9: 31-39.
24. DiNapoli VA, Huber JD, Houser K, et al. Early disruptions of the blood-brain barrier may contribute to exacerbated neuronal damage and prolonged functional recovery following stroke in aged rats. Neurobiol Aging 2008; 29: 753-764.
25. Carmichael ST. Cellular and molecular mechanisms of neural repair after stroke: making waves. Ann Neurol 2006; 59: 735-742.
26. Brown CE, Li P, Boyd JD, et al. Extensive turnover of dendritic spines and vascular remodeling in cortical tissues recovering from stroke. J Neurosci 2007; 27: 4101-4109.
27. Seto A, Taylor S, Trudeau D, et al. Induction of ischemic stroke in awake freely moving mice reveals that isoflurane anesthesia can mask the benefits of a neuroprotection therapy. Front Neuroenergetics 2014; 6: 1.
28. Garbuzova-Davis S, Rodrigues MC, Hernandez-Ontiveros DG, et al. Blood-brain barrier alterations provide evidence of subacute diaschisis in an ischemic stroke rat model. PLoS One 2013; 8: e63553.
29. Hazama F, Ozaki T and Amano S. Scanning electron microscopic study of endothelial cells of cerebral arteries from spontaneously hypertensive rats. Stroke 1979; 10: 245-252.
30. Lam CK, Yoo T, Hiner B, et al. Embolus extravasation is an alternative mechanism for cerebral microvascular recanalization. Nature 2010; 465: 478-482.
31. Armulik A, Genove G and Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 2011; 21: 193-215.
32. Sims DE. The pericyte?a review. Tissue Cell 1986; 18: 153-174.
33. Pluta R, Lossinsky AS, Wisniewski HM, et al. Early blood-brain barrier changes in the rat following transient complete cerebral ischemia induced by cardiac arrest. Brain Res 1994; 633: 41-52.
34. Kajihara H, Tsutsumi E, Kinoshita A, et al. Activated astrocytes with glycogen accumulation in ischemic penumbra during the early stage of brain infarction: immunohistochemical and electron microscopic studies. Brain Res 2001; 909: 92-101.
35. Stewart PA, Magliocco M, Hayakawa K, et al. A quantitative analysis of blood-brain barrier ultrastructure in the aging human. Microvasc Res 1987; 33: 270-282.
36. Alba C, Vidal L, Diaz F, et al. Ultrastructural and quantitative age-related changes in capillaries of the dorsal lateral geniculate nucleus. Brain Res Bull 2004; 64: 145-153.
37. Hicks P, Rolsten C, Brizzee D, et al. Age-related changes in rat brain capillaries. Neurobiol Aging 1983; 4: 69-75.
38. Witt KA, Mark KS, Hom S, et al. Effects of hypoxiareoxygenation on rat blood-brain barrier permeability and tight junctional protein expression. Am J Physiol Heart Circ Physiol 2003; 285: H2820-H2831.
39. Ueno M, Tomita S, Nakagawa T, et al. Effects of aging and HIF-1alpha deficiency on permeability of hippocampal vessels. Microsc Res Tech 2006; 69: 29-35.
40. Broadwell RD, Balin BJ and Salcman M. Transcytotic pathway for blood-borne protein through the bloodbrain barrier. Proc Natl Acad Sci USA 1988; 85: 632-636.
41. Nedergaard M, Jakobsen J and Diemer NH. Autoradiographic determination of cerebral glucose content, blood flow, and glucose utilization in focal ischemia of the rat brain: influence of the plasma glucose concentration. J Cereb Blood Flow Metab 1988; 8: 100-108.