Delayed transplantation of human marrow stromal cell-seeded scaffolds increases transcallosal neural fiber length, angiogenesis, and hippocampal neuronal survival and improves functional outcome after traumatic brain injury in rats

Brain Research

Volumn 1263, Issue , 2009, Pages 183-191

  Xiong, Ye ^a   Qu, Changsheng ^a   Mahmood, Asim ^a   Liu, Zhongwu ^b   Ning, Ruizhuo ^a   Li, Yi ^b   Kaplan, David L ^c   Schallert, Timothy ^d   Chopp, Michael ^b,e  

^a HENRY FORD HEALTH SYSTEM   (United States)

^b HENRY FORD HOSPITAL   (United States)

^c Tufts University   (United States)

^d UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^e OAKLAND UNIVERSITY   (United States)

Author keywords

Angiogenesis; Human bone marrow stromal cell; Neural fiber length; Scaffold; Sensorimotor; Spatial learning; Traumatic brain injury

Indexed keywords

1,1'' DIOLEYL 3,3,3'',3'' TETRAMETHYLINDOCARBOCYANINE METHANESULFONATE; COLLAGEN; MESYLIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW TRANSPLANTATION; BRAIN CORTEX; BRAIN SIZE; CELL LABELING; CELL SURVIVAL; CELL TRANSPLANTATION; CONTROLLED STUDY; HIPPOCAMPUS; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORIMOTOR FUNCTION; SPATIAL DISCRIMINATION; TRAUMATIC BRAIN INJURY; TREATMENT OUTCOME;

ANIMALS; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; BRAIN INJURIES; CELL SURVIVAL; CEREBRAL CORTEX; COLLAGEN; HIPPOCAMPUS; HUMANS; LEARNING; MALE; NEOVASCULARIZATION, PHYSIOLOGIC; NEURONS; RATS; RATS, WISTAR; RECOVERY OF FUNCTION; SPACE PERCEPTION; STROMAL CELLS; TIME FACTORS; TISSUE SCAFFOLDS;

RATTUS;

EID: 61849183079     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.01.032     Document Type: Article

References (35)

1. Rehabilitation of persons with traumatic brain injury. NIH Consens. Statement 16 (1998) 1-41
2. Bakshi A., Fisher O., Dagci T., Himes B.T., Fischer I., and Lowman A. Mechanically engineered hydrogel scaffolds for axonal growth and angiogenesis after transplantation in spinal cord injury. J. Neurosurg. Spine 1 (2004) 322-329
3. Chen J., and Chopp M. Neurorestorative treatment of stroke: cell and pharmacological approaches. NeuroRx 3 (2006) 466-473
4. Chen J., Sanberg P.R., Li Y., Wang L., Lu M., Willing A.E., Sanchez-Ramos J., and Chopp M. Intravenous administration of human umbilical cord blood reduces behavioral deficits after stroke in rats. Stroke 32 (2001) 2682-2688
5. Chen J., Li Y., Zhang R., Katakowski M., Gautam S.C., Xu Y., Lu M., Zhang Z., and Chopp M. Combination therapy of stroke in rats with a nitric oxide donor and human bone marrow stromal cells enhances angiogenesis and neurogenesis. Brain Res. 1005 (2004) 21-28
6. Choi S.H., Woodlee M.T., Hong J.J., and Schallert T. A simple modification of the water maze test to enhance daily detection of spatial memory in rats and mice. J. Neurosci. Methods 156 (2006) 182-193
7. Chopp M., and Li Y. Treatment of neural injury with marrow stromal cells. Lancet Neurol. 1 (2002) 92-100
8. Dixon C.E., Clifton G.L., Lighthall J.W., Yaghmai A.A., and Hayes R.L. A controlled cortical impact model of traumatic brain injury in the rat. J. Neurosci. Methods 39 (1991) 253-262
9. Li Y., Chen J., Chen X.G., Wang L., Gautam S.C., Xu Y.X., Katakowski M., Zhang L.J., Lu M., Janakiraman N., and Chopp M. Human marrow stromal cell therapy for stroke in rat: neurotrophins and functional recovery. Neurology 59 (2002) 514-523
10. Li Y., Chen J., Zhang C.L., Wang L., Lu D., Katakowski M., Gao Q., Shen L.H., Zhang J., Lu M., and Chopp M. Gliosis and brain remodeling after treatment of stroke in rats with marrow stromal cells. Glia 49 (2005) 407-417
11. Liu Z., Li Y., Qu R., Shen L., Gao Q., Zhang X., Lu M., Savant-Bhonsale S., Borneman J., and Chopp M. Axonal sprouting into the denervated spinal cord and synaptic and postsynaptic protein expression in the spinal cord after transplantation of bone marrow stromal cell in stroke rats. Brain Res. 1149 (2007) 172-180
12. Lu D., Li Y., Wang L., Chen J., Mahmood A., and Chopp M. Intraarterial administration of marrow stromal cells in a rat model of traumatic brain injury. J. Neurotrauma 18 (2001) 813-819
13. Lu D., Mahmood A., and Chopp M. Biologic transplantation and neurotrophin-induced neuroplasticity after traumatic brain injury. J. Head Trauma Rehabil. 18 (2003) 357-376
14. Lu D., Mahmood A., Qu C., Goussev A., Schallert T., and Chopp M. Erythropoietin enhances neurogenesis and restores spatial memory in rats after traumatic brain injury. J. Neurotrauma 22 (2005) 1011-1017
15. Lu D., Mahmood A., Qu C., Hong X., Kaplan D., and Chopp M. Collagen scaffolds populated with human marrow stromal cells reduce lesion volume and improve functional outcome after traumatic brain injury. Neurosurgery 61 (2007) 596-602 (discussion 602-3)
16. Lu D., Qu C., Goussev A., Jiang H., Lu C., Schallert T., Mahmood A., Chen J., Li Y., and Chopp M. Statins increase neurogenesis in the dentate gyrus, reduce delayed neuronal death in the hippocampal CA3 region, and improve spatial learning in rat after traumatic brain injury. J. Neurotrauma 24 (2007) 1132-1146
17. Mahmood A., Lu D., Wang L., Li Y., Lu M., and Chopp M. Treatment of traumatic brain injury in female rats with intravenous administration of bone marrow stromal cells. Neurosurgery 49 (2001) 1196-1203 (discussion 1203-4)
18. Mahmood A., Lu D., Yi L., Chen J.L., and Chopp M. Intracranial bone marrow transplantation after traumatic brain injury improving functional outcome in adult rats. J. Neurosurg. 94 (2001) 589-595
19. Mahmood A., Lu D., and Chopp M. Marrow stromal cell transplantation after traumatic brain injury promotes cellular proliferation within the brain. Neurosurgery 55 (2004) 1185-1193
20. Mahmood A., Lu D., Qu C., Goussev A., and Chopp M. Human marrow stromal cell treatment provides long-lasting benefit after traumatic brain injury in rats. Neurosurgery 57 (2005) 1026-1031 (discussion 1026-31)
21. Narayan R.K., Michel M.E., Ansell B., Baethmann A., Biegon A., Bracken M.B., Bullock M.R., Choi S.C., Clifton G.L., Contant C.F., Coplin W.M., Dietrich W.D., Ghajar J., Grady S.M., Grossman R.G., Hall E.D., Heetderks W., Hovda D.A., Jallo J., Katz R.L., Knoller N., Kochanek P.M., Maas A.I., Majde J., Marion D.W., Marmarou A., Marshall L.F., McIntosh T.K., Miller E., Mohberg N., Muizelaar J.P., Pitts L.H., Quinn P., Riesenfeld G., Robertson C.S., Strauss K.I., Teasdale G., Temkin N., Tuma R., Wade C., Walker M.D., Weinrich M., Whyte J., Wilberger J., Young A.B., and Yurkewicz L. Clinical trials in head injury. J. Neurotrauma 19 (2002) 503-557
22. Park K.I., Teng Y.D., and Snyder E.Y. The injured brain interacts reciprocally with neural stem cells supported by scaffolds to reconstitute lost tissue. Nat. Biotechnol. 20 (2002) 1111-1117
23. Paxinos G., and Watson C. The Rat Brain in Stereotactic Coordinates. 2nd ed. (1986), Academic Press, San Diego
24. Potter W., Kalil R.E., and Kao W.J. Biomimetic material systems for neural progenitor cell-based therapy. Front. Biosci. 13 (2008) 806-821
25. Qu C., Mahmood A., Lu D., Goussev A., Xiong Y., and Chopp M. Treatment of traumatic brain injury in mice with marrow stromal cells. Brain Res. 1208 (2008) 234-239
26. Royo N.C., Shimizu S., Schouten J.W., Stover J.F., and McIntosh T.K. Pharmacology of traumatic brain injury. Curr. Opin. Pharmacol. 3 (2003) 27-32
27. Shen L.H., Li Y., Chen J., Zacharek A., Gao Q., Kapke A., Lu M., Raginski K., Vanguri P., Smith A., and Chopp M. Therapeutic benefit of bone marrow stromal cells administered 1 month after stroke. J. Cereb. Blood Flow Metab. 27 (2007) 6-13
28. Swanson R.A., Morton M.T., Tsao-Wu G., Savalos R.A., Davidson C., and Sharp F.R. A semiautomated method for measuring brain infarct volume. J. Cereb. Blood Flow Metab. 10 (1990) 290-293
29. Urdzikova L., Jendelova P., Glogarova K., Burian M., Hajek M., and Sykova E. Transplantation of bone marrow stem cells as well as mobilization by granulocyte-colony stimulating factor promotes recovery after spinal cord injury in rats. J. Neurotrauma 23 (2006) 1379-1391
30. Wright K.T., El Masri W., Osman A., Roberts S., Chamberlain G., Ashton B.A., and Johnson W.E. Bone marrow stromal cells stimulate neurite outgrowth over neural proteoglycans (CSPG), myelin associated glycoprotein and Nogo-A. Biochem. Biophys. Res. Commun. 354 (2007) 559-566
31. Xiong Y., Mahmood A., Lu D., Qu C., Goussev A., Schallert T., and Chopp M. Role of gender in outcome after traumatic brain injury and therapeutic effect of erythropoietin in mice. Brain Res. 1185 (2007) 301-312
32. Xiong Y., Lu D., Qu C., Goussev A., Schallert T., Mahmood A., and Chopp M. Effects of erythropoietin on reducing brain damage and improving functional outcome after traumatic brain injury in mice. J. Neurosurg. 109 (2008) 510-521
33. Zhang R.L., Zhang Z.G., Zhang L., and Chopp M. Proliferation and differentiation of progenitor cells in the cortex and the subventricular zone in the adult rat after focal cerebral ischemia. Neuroscience 105 (2001) 33-41
34. Zhang R., Wang Y., Zhang L., Zhang Z., Tsang W., Lu M., Zhang L., and Chopp M. Sildenafil (Viagra) induces neurogenesis and promotes functional recovery after stroke in rats. Stroke 33 (2002) 2675-2680
35. Zhang C., Li Y., Chen J., Gao Q., Zacharek A., Kapke A., and Chopp M. Bone marrow stromal cells upregulate expression of bone morphogenetic proteins 2 and 4, gap junction protein connexin-43 and synaptophysin after stroke in rats. Neuroscience 141 (2006) 687-695