Effect of vascular endothelial growth factor treatment in experimental traumatic spinal cord injury: In vivo longitudinal assessment

Journal of Neurotrauma

Volumn 28, Issue 4, 2011, Pages 565-578

  Sundberg, Laura M ^a   Herrera, Juan J ^a   Narayana, Ponnada A ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

behavioral assays; diffusion tensor imaging; magnetic resonance imaging; spinal cord injury; vascular endothelial growth factor

Indexed keywords

BUPRENORPHINE; ENROFLOXACIN; VASCULOTROPIN;

ACUTE DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MALE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OLIGODENDROGLIA; RAT; REMYELINIZATION; SPINAL CORD INJURY; TREATMENT OUTCOME;

ANIMALS; AXONS; CELL DIFFERENTIATION; IMMUNOHISTOCHEMISTRY; MAGNETIC RESONANCE IMAGING; MALE; MOTOR ACTIVITY; NERVE FIBERS, MYELINATED; OLIGODENDROGLIA; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SPINAL CORD; SPINAL CORD INJURIES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 79953829608     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2010.1533     Document Type: Article

References (58)

1. Basso, D.M., Beattie, M.S.,and Bresnahan, J.C. (1995). A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 12, 1-21.
2. Beattie, M.S., Hermann, G.E., Rogers, R.C., and Bresnahan, J.C. (2002). Cell death in models of spinal cord injury. Prog. Brain Res. 137, 37-47. (Pubitemid 35460935)
3. Benton, R.L., and Whittemore, S.R. (2003). VEGF165 therapy exacerbates secondary damage following spinal cord injury. Neurochem. Res. 28, 1693-1703. (Pubitemid 37296211)
4. Bockhorst, K.H., Hui, C.K., and Narayana, P.A. (2010a). Fully automatic postprocessing and evaluation of DTI Data: Un-supervised pipeline for batch jobs, in: 18th Annual Meeting of the International Society for Magnetic Resonance in Medicine. Stockholm, Sweden.
5. Bockhorst, K.H., Narayana, P.A., Dulin, J., Liu, R., Rea, H.C., Hahn, K., Wosik, J., and Perez-Polo, J.R. (2010b). Normobaric hyperoximia increases hypoxia-induced cerebral injury: DTI study in rats. J. Neurosci. Res. 88, 1146-1156.
6. Bockhorst, K.H., Narayana, PA., Liu, R, Ahobila-Vijjula, P., Ramu, J., Kamel, M., Wosik, J., Bockhorst, T., Hahn, K., Hasan, K.M., and Perez-Polo, J.R. (2008). Early postnatal development of rat brain: in vivo diffusion tensor imaging. J. Neurosci. Res. 86, 1520-1528. (Pubitemid 351642445)
7. Bresnahan, J.C., Beattie, M.S., Todd, F.D., 3rd, and Noyes, D.H. (1987). A behavioral and anatomical analysis of spinal cord injury produced by a feedback-controlled impaction device. Exp. Neurol. 95, 548-570. (Pubitemid 17046222)
8. Brockington, A., Lewis, C., Wharton, S., and Shaw, P.J. (2004). Vascular endothelial growth factor and the nervous system. Neuropathol. Appl. Neurobiol. 30, 427-446. (Pubitemid 39423031)
9. Budde, M.D., Kim, J.H., Liang, H.F., Schmidt, R.E., Russell, J.H., Cross, A.H., and Song, S.K. (2007). Toward accurate diagnosis of white matter pathology using diffusion tensor imaging. Magn. Reson. Med. 57, 688-695. (Pubitemid 46731794)
10. Budde, M.D., Xie, M., Cross, A.H., and Song, S.K. (2009). Axial diffusivity is the primary correlate of axonal injury in the ex-perimental autoimmune encephalomyelitis spinal cord: a quantitative pixelwise analysis. J. Neurosci. 29, 2805-2813.
11. Cohen, D.M., Patel, C.B., Ahobila-Vajjula, P., Sundberg, L.M., Chacko, T., Liu, S.J., and Narayana, P.A. (2009). Blood-spinal cord barrier permeability in experimental spinal cord injury: dynamic contrast-enhanced MRI. NMR Biomed. 22, 332-341.
12. DeBoy, C.A., Zhang, J., Dike, S., Shats, I., Jones, M., Reich, D.S., Mori, S., Nguyen, T., Rothstein, B., Miller, R.H., Griffin, J.T., Kerr, D.A., and Calabresi, P.A. (2007). High resolution diffu-sion tensor imaging of axonal damage in focal inflammatory and demyelinating lesions in rat spinal cord. Brain 130, 2199-2210. (Pubitemid 47236617)
13. Demediuk, P., Saunders, R.D., Anderson, D.K., Means, E.D., and Horrocks, L.A. (1987). Early membrane lipid changes in la-minectomized and traumatized cat spinal cord. Neurochem. Pathol. 7, 79-89.
14. Deo, A.A., Grill, RJ., Hasan, K.M., and Narayana, P.A. (2006). In vivo serial diffusion tensor imaging of experimental spinal cord injury. J. Neurosci. Res. 83, 801-810.
15. Dijkers, M., Bryce, T., and Zanca, J. (2009). Prevalence of chronic pain after traumatic spinal cord injury: a systematic review. J. Rehabil. Res. Dev. 46, 13-29.
16. Facchiano, F., Fernandez, E., Mancarella, S., Maira, G., Miscusi, M., D'Arcangelo, D., Cimino-Reale, G., Falchetti, M.L., Ca-pogrossi, M.C., and Pallini, R. (2002). Promotion of regenera-tion of corticospinal tract axons in rats with recombinant vascular endothelial growth factor alone and combined with adenovirus coding for this factor. J. Neurosurg. 97, 161-168. (Pubitemid 34693714)
17. Fenyes, D.A., and Narayana, P.A. (1998). In vivo echo-planar imaging of rat spinal cord. Magn. Reson. Imaging 16, 1249-1255. (Pubitemid 29019550)
18. Ferrara, N., Gerber, H.P., and LeCouter, J. (2003). The biology of VEGF and its receptors. Nat. Med. 9, 669-676. (Pubitemid 36749215)
19. Goldsmith, H.S. (1999). Acute spinal cord injuries: a search for functional improvement. Surg. Neurol. 51, 231-233. (Pubitemid 29095868)
20. Hagg, T., and Oudega, M. (2006). Degenerative and spontaneous regenerative processes after spinal cord injury. J. Neurotrauma 23, 264-280. (Pubitemid 43726309)
21. Hahn, K., Prigarin, S., and Hasan, K. (2004). A novel denoising technique for very noisy DTI data, in: The International So-ciety for Magnetic Resonance in Medicine. Kyoto, Japan, p. 1208.
22. 3 resolution, in: The International Society for Magnetic Resonance in Medicine. Miami, Florida, p. 161.
23. Harsan, L.A., Poulet, P., Guignard, B., Steibel, J., Parizel, N., de Sousa, P.L., Boehm, N., Grucker, D., and Ghandour, M.S. (2006). Brain dysmyelination and recovery assessment by noninvasive in vivo diffusion tensor magnetic resonance im-aging. J. Neurosci. Res. 83, 392-402. (Pubitemid 43184403)
24. Herrera, J.J., Nesic-Taylor, D.O., and Narayana, P.A. (2009). Reduced vascular endothelial growth factor expression in contusive spinal cord injury. J Neurotrauma 26, 995-1003.
25. Jiang, H., van Zijl, P.C., Kim, J., Pearlson, G.D., and Mori, S. (2006). DtiStudio: resource program for diffusion tensor computation and fiber bundle tracking. Comput. Methods Programs Biomed. 81, 106-116. (Pubitemid 43144442)
26. Kim, H.M., Hwang, D.H., Lee, J.E., Kim, S.U., and Kim, B.G (2009). Ex vivo VEGF delivery by neural stem cells enhances proliferation of glial progenitors, angiogenesis, and tissue sparing after spinal cord injury. PLoS One. 4, e4987.
27. Kozlowski, P., Raj, D., Liu, J., Lam, C., Yung, A.C., and Tetzlaff, W. (2008). Characterizing white matter damage in rat spinal cord with quantitative MRI and histology. J. Neurotrauma 25, 653-676. (Pubitemid 351918437)
28. Madi, S., Hasan, K.M., and Narayana, P.A. (2005). Diffusion tensor imaging of in vivo and excised rat spinal cord at 7 T with an icosahedral encoding scheme. Magn. Reson. Med. 53, 118-125. (Pubitemid 40110484)
29. Mihai, G., Nout, Y.S., Tovar, C.A., Miller, B.A., Schmalbrock, P., Bresnahan, J.C., and Beattie, M.S. (2008). Longitudinal com-parison of two severities of unilateral cervical spinal cord injury using magnetic resonance imaging in rats. J. Neuro-trauma 25, 1-18. (Pubitemid 351161067)
30. Mills, C.D., Grady, J.J., and Hulsebosch, C.E. (2001). Changes in exploratory behavior as a measure of chronic central pain following spinal cord injury. J. Neurotrauma 18, 1091-1105. (Pubitemid 33000678)
31. Nesic-Taylor, D.O., Sundberg, L.M., Herrera, J.J., Mokkapati, V.U., Lee, J., and Narayana, P.A. (2010). VEGF and spinal cord injury pain. J. Neurotrauma 27, 1793-1803.
32. 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)
33. Nolan, RT. (1969). Traumatic oedema of the spinal cord. Br. Med. J. 1, 710.
34. Otrock, Z.K., Mahfouz, R.A., Makarem, J.A., and Shamseddine, A.I. (2007). Understanding the biology of angiogenesis: review of the most important molecular mechanisms. Blood Cells Mol. Dis. 39, 212-220. (Pubitemid 47126926)
35. Patel, C.B., Cohen, D.M., Ahobila-Vajjula, P., Sundberg, L.M., Chacko, T., and Narayana, P.A. (2009). Effect of VEGF treatment on the blood-spinal cord barrier perme-ability in experimental spinal cord injury: Dynamic contrast-enhanced magnetic resonance imaging. J. Neurotrauma 26, 1005-1016.
36. Peng, X.M., Zhou, ZG., Glorioso, J.C., Fink, D.J., and Mata, M. (2006). Tumor necrosis factor-alpha contributes to below-level neuropathic pain after spinal cord injury. Ann. Neurol. 59, 843-851. (Pubitemid 43673162)
37. Profyris, C., Cheema, S.S., Zang, D., Azari, M.F., Boyle, K., and Petratos, S. (2004). Degenerative and regenerative mechanisms governing spinal cord injury. Neurobiol. Dis. 15, 415-436. (Pubitemid 38429958)
38. Reulen, H.J., Graham, R., Spatz, M., and Klatzo, I. (1977). Role of pressure gradients and bulk flow in dynamics of vasogenic brain edema. J. Neurosurg. 46, 24-35. (Pubitemid 8013270)
39. Reulen, H.J. (1976). Vasogenic brain oedema. New aspects in its formation, resolution and therapy. Br. J. Anaesth. 48, 741-752.
40. Rivlin, A.S., and Tator, C.H. (1977). Objective clinical assessment of motor function after experimental spinal cord injury in the rat. J. Neurosurg. 47, 577-581. (Pubitemid 8193904)
41. Rosenstein, J.M., and Krum, J.M. (2004). New roles for VEGF in nervous tissue\beyond blood vessels. Exp. Neurol. 187, 246-253. (Pubitemid 38610271)
42. Sharma, H.S. (2005). Pathophysiology of blood-spinal cord bar-rier in traumatic injury and repair. Curr. Pharm. Des. 11, 1353-1389. (Pubitemid 40598002)
43. Sondell, M., Lundborg, G., and Kanje, M. (1999). Vascular en-dothelial growth factor has neurotrophic activity and stimu-lates axonal outgrowth., enhancing cell survival and Schwann cell proliferation in the peripheral nervous system. J. Neurosci. 19, 5731-5740. (Pubitemid 29327910)
44. Sondell, M., Sundler, F., and Kanje, M. (2000). Vascular endo-thelial growth factor is a neurotrophic factor which stimulates axonal outgrowth through the flk-1 receptor. Eur. J. Neurosci. 12, 4243-4254. (Pubitemid 32037835)
45. Song, S.K., Sun, S.W., Ramsbottom, M.J., Chang, C., Russell, J., and Cross, A.H. (2002). Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17, 1429-1436. (Pubitemid 35333862)
46. Song, S.K., Yoshino, J., Le, T.Q., Lin, S.J., Sun, S.W., Cross, A.H., and Armstrong, RC. (2005). Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 26, 132-140. (Pubitemid 40602893)
47. Storkebaum, E., Lambrechts, D., and Carmeliet, P. (2004). VEGF: Once regarded as a specific angiogenic factor, now implicated in neuroprotection. Bioessays 26, 943-954. (Pubitemid 39273068)
48. Sundberg, L.M., Herrera, J.J., and Narayana, P.A. (2010). In vivo longitudinal MRI and behavioral studies in experimental spinal cord injury. J. Neurotrauma 27, 1753-1767
49. Tammela, T., Enholm, B., Alitalo, K., and Paavonen, K. (2005). The biology of vascular endothelial growth factors. Cardio-vasc Res. 65, 550-563. (Pubitemid 40138976)
50. Twisk, J., and de Vente, W. (2002). Attrition in longitudinal studies. How to deal with missing data. J. Clin. Epidemiol. 55, 329-337. (Pubitemid 34240484)
51. van Neerven, S., Joosten, E.A., Brook, GA., Lambert, C.A., Mey, J., Weiss, J., Marcus, M.A., Steinbusch, H.W., van Kleef, M., Patijn, J., and Deumens, R. (2010). Repetitive intrathecal VEGF165 treatment has limited therapeutic effects after spinal cord injury in the rat. J. Neurotrauma 27, 1781-1791.
52. Weirich, S.D., Cotler, H.B., Narayana, PA., Hazle, J.D., Jackson E.F., Coupe, K.J., McDonald, C.L., Langford, L.A., and Harris, J.H., Jr. (1990). Histopathologic correlation of magnetic reso-nance imaging signal patterns in a spinal cord injury model. Spine 15, 630-638. (Pubitemid 20264748)
53. Widenfalk, J., Lipson, A., Jubran, M., Hofstetter, C., Ebendal, T., Cao, Y., and Olson, L. (2003). Vascular endothelial growth factor improves functional outcome and decreases secondary degeneration in experimental spinal cord contusion injury. Neuroscience 120, 951-960. (Pubitemid 36966647)
54. Woods, R.P., Grafton, S.T., Holmes, C.J., Cherry, S.R., and Mazziotta, J.C. (1998). Automated image registration: I. Gen-eral methods and intrasubject, intramodality validation. J. Comput. Assist. Tomogr. 22, 139-152. (Pubitemid 28087337)
55. Yashon, D., Bingham, W.G, Jr., Faddoul, E.M., and Hunt, W.E. (1973). Edema of the spinal cord following experimental im-pact trauma. J. Neurosurg. 38, 693-697
56. Ye, F., and Xiang, Q.-S. (2007). Digital tuning to suppress ghost artifacts in EPI by minimization of total variation, in: The In-ternational Society for Magnetic Resonance in Medicine. Ber-lin, Germany, p. 1841.
57. Zachary, I. (2005). Neuroprotective role of vascular endo-thelial growth factor: signalling mechanisms, biological function, and therapeutic potential. Neurosignals 14, 207-221. (Pubitemid 41661355)
58. Zhang, Z.G., Zhang, L., Jiang, Q., Zhang, R., Davies, K., Powers, C., Bruggen, N., and Chopp, M. (2000). VEGF enhances an-giogenesis and promotes blood-brain barrier leakage in the ischemic brain. J. Clin. Invest. 106, 829-838.