Intrathecal transplantation of bone marrow stromal cells attenuates blood-spinal cord barrier disruption induced by spinal cord ischemia-reperfusion injury in rabbits

Journal of Vascular Surgery

Volumn 58, Issue 4, 2013, Pages 1043-1052

  Fang, Bo ^a   Wang, He ^a   Sun, Xue Jun ^a   Li, Xiao Qian ^a   Ai, Chun Yu ^a   Tan, Wen Fei ^a   White, Paul F ^b,c   Ma, Hong ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b CEDARS SINAI MEDICAL CENTER   (United States)

^c White Mountain Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE B; TIGHT JUNCTION PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AORTA OCCLUSION; ARTICLE; BLOOD SPINAL CORD BARRIER DISRUPTION; HINDLIMB; MOTOR PERFORMANCE; NONHUMAN; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; REPERFUSION INJURY; SPINAL CORD INJURY; STEM CELL TRANSPLANTATION; TISSUE SECTION;

ANIMALS; BONE MARROW TRANSPLANTATION; CAPILLARY PERMEABILITY; CELLS, CULTURED; DISEASE MODELS, ANIMAL; HINDLIMB; INJECTIONS, SPINAL; MATRIX METALLOPROTEINASE 9; MOTOR ACTIVITY; MOTOR NEURONS; MUSCLE, SKELETAL; OCCLUDIN; RABBITS; REPERFUSION INJURY; SPINAL CORD; STROMAL CELLS; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84884909506     PISSN: 07415214     EISSN: 10976809     Source Type: Journal    
DOI: 10.1016/j.jvs.2012.11.087     Document Type: Article

References (40)

1. V.I. Patel, E. Ergul, M.F. Conrad, M. Cambria, G.M. LaMuraglia, and C.J. Kwolek Continued favorable results with open surgical repair of type IV thoracoabdominal aortic aneurysms J Vasc Surg 53 2011 1492 1498
2. M.F. Conrad, J.Y. Ye, T.K. Chung, J.K. Davison, and R.P. Cambria Spinal cord complications after thoracic aortic surgery: long-term survival and functional status varies with deficit severity J Vasc Surg 48 2008 47 53
3. C.P. Hofstetter, E.J. Schwarz, D. Hess, J. Widenfalk, A. El Manira, and D.J. Prockop Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery Proc Natl Acad Sci U S A 99 2002 2199 2204
4. B. Neuhuber, B. Timothy Himes, J.S. Shumsky, G. Gallo, and I. Fischer Axon growth and recovery of function supported by human bone marrow stromal cells in the injured spinal cord exhibit donor variations Brain Res 1035 2005 73 85
5. E. Shi, T. Kazui, X. Jiang, N. Washiyama, K. Yamashita, and H. Terada Intrathecal injection of bone marrow stromal cells attenuates neurologic injury after spinal cord ischemia Ann Thorac Surg 81 2006 2227 2233
6. E. Shi, T. Kazui, X. Jiang, N. Washiyama, K. Yamashita, and H. Terada Therapeutic benefit of intrathecal injection of marrow stromal cells on ischemia-injured spinal cord Ann Thorac Surg 83 2007 1484 1490
7. M. Koda, T. Kamada, M. Hashimoto, M. Murakami, H. Shirasawa, and S. Sakao Adenovirus vector-mediated ex vivo gene transfer of brain-derived neurotrophic factor to bone marrow stromal cells promotes axonal regeneration after transplantation in completely transected adult rat spinal cord Eur Spine J 16 2007 2206 2214
8. V.R. Dasari, D.G. Spomar, C. Cady, M. Gujrati, J.S. Rao, and D.H. Dinh Mesenchymal stem cells from rat bone marrow downregulate caspase-3-mediated apoptotic pathway after spinal cord injury in rats Neurochem Res 32 2007 2080 2093
9. J.T. Maikos, and D.I. Shreiber Immediate damage to the blood-spinal cord barrier due to mechanical trauma J Neurotrauma 24 2007 492 507
10. L.J. Noble, F. Donovan, T. Igarashi, S. Goussev, and Z. Werb Matrix metalloproteinases limit functional recovery after spinal cord injury by modulation of early vascular events J Neurosci 22 2002 7526 7535
11. L. Mao, H. Wang, L. Qiao, and X. Wang Disruption of Nrf2 enhances the upregulation of nuclear factor-kappaB activity, tumor necrosis factor-α, and matrix metalloproteinase-9 after spinal cord injury in mice Mediators Inflamm 2010 2010 238321
12. H.S. Sharma Pathophysiology of blood-spinal cord barrier in traumatic injury and repair Curr Pharm Des 11 2005 1353 1389
13. C.V. Borlongan, J.G. Lind, O. Dillon-Carter, G. Yu, M. Hadman, and C. Cheng Bone marrow grafts restore cerebral blood flow and blood brain barrier in stroke rats Brain Res 1010 2004 108 116
14. T. Hirase, J.M. Staddon, M. Saitou, Y. Ando-Akatsuka, M. Itoh, and M. Furuse Occludin as a possible determinant of tight junction permeability in endothelial cells J Cell Sci 110 1997 1603 1613
15. S.A. Wexler, C. Donaldson, P. Denning-Kendall, C. Rice, B. Bradley, and J.M. Hows Adult bone marrow is a rich source of human mesenchymal 'stem' cells but umbilical cord and mobilized adult blood are not Br J Haematol 121 2003 368 374
16. I.M. Tarlov Spinal cord compression: mechanisms of paralysis and treatment 1957 Charles C Thomas Springfield, IL p 147
17. T.S. Westvik, T.N. Fitzgerald, A. Muto, S.P. Maloney, J.M. Pimiento, and T.T. Fancher Limb ischemia after iliac ligation in aged mice stimulates angiogenesis without arteriogenesis J Vasc Surg 49 2009 464 473
18. G.S. Maharajh, E.A. Pascoe, W.C. Halliday, H.P. Grocott, D.B. Thiessen, and L.G. Girling Neurological outcome in a porcine model of descending thoracic aortic surgery. Left atrial femoral artery bypass versus clamp and repair Stroke 27 1996 2095 2100 discussion 2101
19. G.R. Ding, L.B. Qiu, X.W. Wang, K.C. Li, Y.C. Zhou, and Y. Zhou EMP-induced alterations of tight junction protein expression and disruption of the blood-brain barrier Toxicol Lett 196 2010 154 160
20. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method Methods 25 2001 402 408
21. M. Strioga, S. Viswanathan, A. Darinskas, O. Slaby, and J. Michalek Same or not the same? Comparison of adipose tissue-derived versus bone marrow-derived mesenchymal stem and stromal cells Stem Cells Dev 21 2012 2724 2752
22. A. Bakshi, C. Hunter, S. Swanger, A. Lepore, and I. Fischer Minimally invasive delivery of stem cells for spinal cord injury: advantages of the lumbar puncture technique J Neurosurg Spine 1 2004 330 337
23. N.J. Abbott, L. Rönnbäck, and E. Hansson Astrocyte-endothelial interactions at the blood-brain barrier Nat Rev Neurosci 7 2006 41 53
24. T.P. Jacobs, O. Kempski, D. McKinley, A.J. Dutka, J.M. Hallenbeck, and G. Feuerstein Blood flow and vascular permeability during motor dysfunction in a rabbit model of spinal cord ischemia Stroke 23 1992 367 373
25. H.S. Sharma New perspectives for the treatment options in spinal cord injury Expert Opin Pharmacother 9 2008 2773 2800
26. J. Liu, X. Jin, K.J. Liu, and W. Liu Matrix metalloproteinase-2-mediated occludin degradation and caveolin-1-mediated claudin-5 redistribution contribute to blood-brain barrier damage in early ischemic stroke stage J Neurosci 32 2012 3044 3057
27. L.J. Noble, and J.R. Wrathall Distribution and time course of protein extravasation in the rat spinal cord after contusive injury Brain Res 482 1989 57 66
28. H.S. Sharma, Y. Olsson, S. Persson, and F. Nyberg Trauma-induced opening of the the blood-spinal cord barrier is reduced by indomethacin, an inhibitor of prostaglandin biosynthesis. Experimental observations in the rat using [131I]-sodium, Evans blue and lanthanum as tracers Restor Neurol Neurosci 7 1995 207 215
29. H. Jiao, Z. Wang, Y. Liu, P. Wang, and Y. Xue Specific role of tight junction proteins claudin-5, occludin, and ZO-1 of the blood-brain barrier in a focal cerebral ischemic insult J Mol Neurosci 44 2011 130 139
30. Y.Z. Qu, M. Li, Y.L. Zhao, Z.W. Zhao, X.Y. Wei, and J.P. Liu Astragaloside IV attenuates cerebral ischemia-reperfusion-induced increase in permeability of the blood-brain barrier in rats Eur J Pharmacol 606 2009 137 141
31. G.A. Rosenberg, E.Y. Estrada, and J.E. Dencoff Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain Stroke 29 1998 2189 2195
32. Y. Yang, E.Y. Estrada, J.F. Thompson, W. Liu, and G.A. Rosenberg Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat J Cereb Blood Flow Metab 27 2007 697 709
33. J. Xiang, R. Lan, Y.P. Tang, Y.P. Chen, and D.F. Cai Apocynum venetum leaf extract attenuates disruption of the blood-brain barrier and upregulation of matrix metalloproteinase-9/-2 in a rat model of cerebral ischemia-reperfusion injury Neurochem Res 37 2012 1820 1828
34. P. Svedin, H. Hagberg, K. Sävman, C. Zhu, and C. Mallard Matrix metalloproteinase-9 gene knock-out protects the immature brain after cerebral hypoxia-ischemia J Neurosci 27 2007 1511 1518
35. A. Vakili, S. Mojarrad, M.M. Akhavan, and A. Rashidy-Pour Pentoxifylline attenuates TNF-α protein levels and brain edema following temporary focal cerebral ischemia in rats Brain Res 1377 2011 119 125
36. W.G. Mayhan Cellular mechanisms by which tumor necrosis factor-alpha produces disruption of the blood-brain barrier Brain Res 927 2002 144 152
37. M.K. Sharief, and E.J. Thompson In vivo relationship of tumor necrosis factor-alpha to blood-brain barrier damage in patients with active multiple sclerosis J Neuroimmunol 38 1992 27 33
38. C. Silwedel, and C. Förster Differential susceptibility of cerebral and cerebellar murine brain microvascular endothelial cells to loss of barrier properties in response to inflammatory stimuli J Neuroimmunol 179 2006 37 45
39. F. Takata, S. Dohgu, J. Matsumoto, H. Takahashi, T. Machida, and T. Wakigawa Brain pericytes among cells constituting the blood-brain barrier are highly sensitive to tumor necrosis factor-α, releasing matrix metalloproteinase-9 and migrating in vitro J Neuroinflammation 8 2011 106
40. Y.J. Kim, H.J. Park, G. Lee, O.Y. Bang, Y.H. Ahn, and E. Joe Neuroprotective effects of human mesenchymal stem cells on dopaminergic neurons through anti-inflammatory action Glia 57 2009 13 23