Characterization of vascular disruption and blood-spinal cord barrier permeability following traumatic spinal cord injury

Journal of Neurotrauma

Volumn 31, Issue 6, 2014, Pages 541-552

  Figley, Sarah A ^a,b   Khosravi, Ramak ^b   Legasto, Jean M ^b   Tseng, Yun Fan ^b   Fehlings, Michael G ^a,b  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Blood spinal cord barrier; endogenous angiogenesis; spinal cord injury; vascular injury; vascular permeability

Indexed keywords

AGGLUTININ; EVANS BLUE; FLUORESCEIN ISOTHIOCYANATE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD SPINAL CORD BARRIER; BLOOD VESSEL INJURY; BLOOD VESSEL PERMEABILITY; CONTROLLED STUDY; ENDOTHELIUM CELL; EPIFLUORESCENCE MICROSCOPY; FEMALE; GRAY MATTER; IMMUNOHISTOCHEMISTRY; MICROVASCULATURE; NONHUMAN; PERMEABILITY BARRIER; RAT; REVASCULARIZATION; SPECTROPHOTOMETRY; SPINAL CORD INJURY; WHITE MATTER;

ANIMALS; BLOOD-BRAIN BARRIER; DISEASE MODELS, ANIMAL; FEMALE; NEOVASCULARIZATION, PATHOLOGIC; PERMEABILITY; RATS; RATS, WISTAR; SPINAL CORD; SPINAL CORD INJURIES; TIME FACTORS;

EID: 84896381322     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2013.3034     Document Type: Article

References (37)

1. Furlan, J.C., and Fehlings, M.G. (2008). Cardiovascular complications after acute spinal cord injury: pathophysiology, diagnosis, and management. Neurosurg. Focus 25, E15.
2. Holtz, A., Nystrom, B., and Gerdin, B. (1990). Relation between spinal cord blood flow and functional recovery after blocking weightinduced spinal cord injury in rats. Neurosurgery 26, 952-957. (Pubitemid 20183230)
3. Loy, D.N., Crawford, C.H., Darnall, J.B., Burke, D.A., Onifer, S.M., and Whittemore, S.R. (2002). Temporal progression of angiogenesis and basal lamina deposition after contusive spinal cord injury in the adult rat. J. Comp. Neurol. 445, 308-324. (Pubitemid 34252854)
4. Tator, C.H., and Koyanagi, I. (1997). Vascular mechanisms in the pathophysiology of human spinal cord injury. J. Neurosurg. 86, 483-492. (Pubitemid 27097095)
5. Benton, R.L., Maddie, M.A., Minnillo, D.R., Hagg, T., and Whittemore, S.R. (2008). Griffonia simplicifolia isolectin B4 identifies a specific subpopulation of angiogenic blood vessels following contusive spinal cord injury in the adult mouse. J. Comp. Neurol. 507, 1031-1052. (Pubitemid 351214227)
6. Engelhardt, B., and Coisne, C. (2011). Fluids and barriers of the CNS establish immune privilege by confining immune surveillance to a two-walled castle moat surrounding the CNS castle. Fluids Barriers CNS 8, 4.
7. Ling, X., and Liu, D. (2007). Temporal and spatial profiles of cell loss after spinal cord injury: reduction by a metalloporphyrin. J. Neurosci. Res. 85, 2175-2185. (Pubitemid 47172149)
8. Liu, X.Z., Xu, X.M., Hu, R., Du, C., Zhang, S.X., McDonald, J.W., Dong, H.X., Wu, Y.J., Fan, G.S., Jacquin, M.F., Hsu, C.Y., and Choi, D.W. (1997). Neuronal and glial apoptosis after traumatic spinal cord injury. J. Neurosci. 17, 5395-5406. (Pubitemid 27300306)
9. Lou, J., Lenke, L.G., Ludwig, F.J., and O'Brien, M.F. (1998). Apoptosis as a mechanism of neuronal cell death following acute experimental spinal cord injury. Spinal Cord 36, 683-690. (Pubitemid 28479074)
10. Ribatti, D., Vacca, A., Nico, B., Roncali, L., and Dammacco, F. (2001). Postnatal vasculogenesis. Mech. Dev. 100, 157-163. (Pubitemid 32109326)
11. Carmeliet, P. (2000). Mechanisms of angiogenesis and arteriogenesis. Nat. Med. 6, 389-395. (Pubitemid 30208155)
12. Glaser, J., Gonzalez, R., Sadr, E., and Keirstead, H.S. (2006). Neutralization of the chemokine CXCL10 reduces apoptosis and increases axon sprouting after spinal cord injury. J. Neurosci. Res. 84, 724-734. (Pubitemid 44366674)
13. Kaneko, S., Iwanami, A., Nakamura, M., Kishino, A., Kikuchi, K., Shibata, S., Okano, H.J., Ikegami, T., Moriya, A., Konishi, O., Nakayama, C., Kumagai, K., Kimura, T., Sato, Y., Goshima, Y., Taniguchi, M., Ito, M., He, Z., Toyama, Y., and Okano, H. (2006). A selective Sema3A inhibitor enhances regenerative responses and functional recovery of the injured spinal cord. Nat. Med. 12, 1380-1389. (Pubitemid 44924496)
14. Yoshihara, T., Ohta, M., Itokazu, Y., Matsumoto, N., Dezawa, M., Suzuki, Y., Taguchi, A., Watanabe, Y., Adachi, Y., Ikehara, S., Sugimoto, H., and Ide, C. (2007). Neuroprotective effect of bone marrow-derived mononuclear cells promoting functional recovery from spinal cord injury. J. Neurotrauma 24, 1026-1036. (Pubitemid 47015436)
15. Ohab, J.J., Fleming, S., Blesch, A., and Carmichael, S.T. (2006). A neurovascular niche for neurogenesis after stroke. J. Neurosci. 26, 13007-13016. (Pubitemid 44954619)
16. Peters, K.G., De Vries, C., and Williams, L.T. (1993). Vascular endothelial growth factor receptor expression during embryogenesis and tissue repair suggests a role in endothelial differentiation and blood vessel growth. Proc. Natl. Acad. Sci. U. S. A. 90, 8915-8919. (Pubitemid 23306421)
17. Raab, S., and Plate, K. (2007). Different networks, common growth factors: shared growth factors and receptors of the vascular and the nervous system. Acta Neuropathol. 113, 607-626. (Pubitemid 46863898)
18. Bearden, S.E., and Segal, S.S. (2004). Microvessels promote motor nerve survival and regeneration through local VEGF release following ectopic reattachment. Microcirculation 11, 633-644. (Pubitemid 40012342)
19. Casella, G.T.B., Marcillo, A., Bunge, M.B., and Wood, P.M. (2002). New vascular tissue rapidly replaces neural parenchyma and vessels destroyed by a contusion injury to the rat spinal cord. Exp. Neurol. 173, 63-76. (Pubitemid 34081726)
20. Schumacher, P.A., Eubanks, J.H., and Fehlings, M.G. (1999). Increased calpain I-mediated proteolysis, and preferential loss of dephosphorylated NF200, following traumatic spinal cord injury. Neuroscience 91, 733-744. (Pubitemid 29193281)
21. von Euler, M., Seiger,A ., and Sundström, E. (1997). Clip compression injury in the spinal cord: a correlative study of neurological and morphological alterations. Exp. Neurol. 145, 502-510. (Pubitemid 27314801)
22. Grossman, S.D., Rosenberg, L.J., and Wrathall, J.R. (2001). Temporal- spatial pattern of acute neuronal and glial loss after spinal cord contusion. Exp. Neurol. 168, 273-282. (Pubitemid 32289763)
23. Tator, C.H., and Fehlings, M.G. (1991). Review of the secondary injury theory of acute spinal cord trauma with emphasis on vascular mechanisms. J. Neurosurg. 75, 15-26.
24. Noble, L.J., and Wrathall, J.R. (1989). Distribution and time course of protein extravasation in the rat spinal cord after contusive injury. Brain Res. 482, 57-66. (Pubitemid 19063150)
25. Noble, L.J., and Wrathall, J.R. (1988). Blood-spinal cord barrier disruption proximal to a spinal cord transection in the rat: time course and pathways associated with protein leakage. Exp. Neurol. 99, 567-578. (Pubitemid 18080762)
26. Noble, L.J., and Wrathall, J.R. (1987). The blood-spinal cord barrier after injury: pattern of vascular events proximal and distal to a transection in the rat. Brain Res. 424, 177-188. (Pubitemid 18043578)
27. Benton, R.L., and Whittemore, S.R. (2003). VEGF165 therapy exacerbates secondary damage following spinal cord injury. Neurochem. Res. 28, 1693-1703. (Pubitemid 37296211)
28. Gruner, J.A. (1992). A monitored contusion model of spinal cord injury in the rat. J. Neurotrauma 9, 123-126.
29. Popovich, P.G., Horner, P.J., Mullin, B.B., and Stokes, B.T. (1996). A quantitative spatial analysis of the blood-spinal cord barrier. I. Permeability changes after experimental spinal contusion injury. Exp. Neurol. 142, 258-275. (Pubitemid 26414059)
30. Fehlings, M.G., and Tator, C.H. (1995). The relationships among the severity of spinal cord injury, residual neurological function, axon counts, and counts of retrogradely labeled neurons after experimental spinal cord injury. Exp. Neurol. 132, 220-228.
31. Ikeda, Y., Wang, M., and Nakazawa, S. (1994). Simple quantitative evaluation of blood-brain barrier disruption in vasogenic brain edema. Acta Neurochir. Suppl. (Wien) 60, 119-120.
32. Saria, A., and Lundberg, J.M. (1983). Evans blue fluorescence: quantitative and morphological evaluation of vascular permeability in animal tissues. J. Neurosci. Methods 8, 41-49. (Pubitemid 13083017)
33. Hagg, T., and Oudega, M. (2006). Degenerative and spontaneous regenerative processes after spinal cord injury. J. Neurotrauma 23, 264-280. (Pubitemid 43726309)
34. Noble, L.J., and Wrathall, J.R. (1989). Distribution and time course of protein extravasation in the rat spinal cord after contusive injury. Brain Res. 482, 57-66. (Pubitemid 19063150)
35. Aoki, T., Sumii, T., Mori, T., Wang, X., and Lo, E.H. (2002). Bloodbrain barrier disruption and matrix metalloproteinase-9 expression during reperfusion injury: mechanical versus embolic focal ischemia in spontaneously hypertensive rats. Stroke 33, 2711-2717. (Pubitemid 35266446)
36. Saunders, N., Habgood, M., and Dziegielewska, K.M. (1999). Barrier mechanisms in the brain, I. Adult brain. Clin. Exp. Pharmacol. Physiol. 26, 11-19.
37. Kaya, M., and Ahishali, B. (2011). Assessment of permeability in barrier type of endothelium in brain using tracers: Evans blue, sodium fluorescein, and horseradish peroxidase. Methods Mol. Biol. 763, 369-382.