Transplanted bone marrow stromal cells improves cognitive dysfunction due to diffuse axonal injury in rats: Original Article

Neuropathology

Volumn 29, Issue 4, 2009, Pages 422-432

  Maruichi, Katsuhiko ^a   Kuroda, Satoshi ^a   Chiba, Yasuhiro ^a   Hokari, Masaaki ^a   Shichinohe, Hideo ^a   Hida, Kazutoshi ^a   Iwasaki, Yoshinobu ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Bone marrow stromal cell; Cognitive function; Differentiation; Diffuse axonal injury; Neuroprotection; Transplantation

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; BONE MARROW STROMA CELL TRANSPLANTATION; CELL TRANSPLANTATION; COGNITIVE DEFECT; CONTROLLED STUDY; DIFFUSE AXONAL INJURY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STROMA CELL; TREATMENT OUTCOME;

ANIMALS; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; BRAIN; CELL MOVEMENT; COGNITION DISORDERS; DIFFUSE AXONAL INJURY; MALE; MICE; MICE, TRANSGENIC; RATS; RATS, SPRAGUE-DAWLEY; STROMAL CELLS;

EID: 67651250942     PISSN: 09196544     EISSN: 14401789     Source Type: Journal    
DOI: 10.1111/j.1440-1789.2008.00995.x     Document Type: Article

References (58)

1. Adams JH, Graham DI, Murray LS, Scott G. Diffuse axonal injury due to nonmissile head injury in humans: an analysis of 45 cases. Ann Neurol 1982 12 : 557 563.
2. Gennarelli TA, Thibault LE, Adams JH, Graham DI, Thompson CJ, Marcincin RP. Diffuse axonal injury and traumatic coma in the primate. Ann Neurol 1982 12 : 564 574.
3. Povlishock JT. Traumatically induced axonal injury: pathogenesis and pathobiological implications. Brain Pathol 1992 2 : 1 12.
4. Azizi SA, Stokes D, Augelli BJ, DiGirolamo C, Prockop DJ. Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats-similarities to astrocyte grafts. Proc Natl Acad Sci USA 1998 95 : 3908 3913.
5. Kopen GC, Prockop DJ, Phinney DG. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc Natl Acad Sci USA 1999 96 : 10711 10716.
6. Woodbury D, Schwarz EJ, Prockop DJ, Black IB. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res 2000 61 : 364 370.
7. Hokari M, Kuroda S, Shichinohe H, Yano S, Hida K, Iwasaki Y. Bone marrow stromal cells protect and repair damaged neurons through multiple mechanisms. J Neurosci Res 2008 86 : 1024 1035.
8. Lu D, Li Y, Mahmood A, Wang L, Rafiq T, Chopp M. Neural and marrow-derived stromal cell sphere transplantation in a rat model of traumatic brain injury. J Neurosurg 2002 97 : 935 940.
9. Lu D, Li Y, Wang L, Chen J, Mahmood A, Chopp M. Intraarterial administration of marrow stromal cells in a rat model of traumatic brain injury. J Neurotrauma 2001 18 : 813 819. (Pubitemid 32769777)
10. Lu D, Mahmood A, Wang L, Li Y, Lu M, Chopp M. Adult bone marrow stromal cells administered intravenously to rats after traumatic brain injury migrate into brain and improve neurological outcome. Neuroreport 2001 12 : 559 563.
11. Lu J, Moochhala S, Moore XL et al. Adult bone marrow cells differentiate into neural phenotypes and improve functional recovery in rats following traumatic brain injury. Neurosci Lett 2006 398 : 12 17.
12. Mahmood A, Lu D, Chopp M. Marrow stromal cell transplantation after traumatic brain injury promotes cellular proliferation within the brain. Neurosurgery 2004 55 : 1185 1193.
13. Mahmood A, Lu D, Lu M, Chopp M. Treatment of traumatic brain injury in adult rats with intravenous administration of human bone marrow stromal cells. Neurosurgery 2003 53 : 697 702 discussion 2 3.
14. Mahmood A, Lu D, Qu C, Goussev A, Chopp M. Human marrow stromal cell treatment provides long-lasting benefit after traumatic brain injury in rats. Neurosurgery 2005 57 : 1026 1031 discussion 26 31.
15. Mahmood A, Lu D, Qu C, Goussev A, Chopp M. Long-term recovery after bone marrow stromal cell treatment of traumatic brain injury in rats. J Neurosurg 2006 104 : 272 277.
16. Mahmood A, Lu D, Wang L, Chopp M. Intracerebral transplantation of marrow stromal cells cultured with neurotrophic factors promotes functional recovery in adult rats subjected to traumatic brain injury. J Neurotrauma 2002 19 : 1609 1617.
17. Mahmood A, Lu D, Wang L, Li Y, Lu M, Chopp M. Treatment of traumatic brain injury in female rats with intravenous administration of bone marrow stromal cells. Neurosurgery 2001 49 : 1196 1203 discussion 203 204.
18. Lu D, Mahmood A, Qu C, Hong X, Kaplan D, Chopp M. Collagen scaffolds populated with human marrow stromal cells reduce lesion volume and improve functional outcome after traumatic brain injury. Neurosurgery 2007 61 : 596 602 discussion 2 3.
19. Mahmood A, Lu D, Qu C, Goussev A, Chopp M. Treatment of traumatic brain injury with a combination therapy of marrow stromal cells and atorvastatin in rats. Neurosurgery 2007 60 : 546 553 discussion 53 54.
20. Cernak I. Animal models of head trauma. NeuroRx 2005 2 : 410 422.
21. Shichinohe H, Kuroda S, Lee JB et al. In vivo tracking of bone marrow stromal cells transplanted into mice cerebral infarct by fluorescence optical imaging. Brain Res Brain Res Protoc 2004 13 : 166 175.
22. Shichinohe H, Kuroda S, Yano S et al. Improved expression of gamma-aminobutyric acid receptor in mice with cerebral infarct and transplanted bone marrow stromal cells: an autoradiographic and histologic analysis. J Nucl Med 2006 47 : 486 491.
23. Shichinohe H, Kuroda S, Tsuji S et al. Bone marrow stromal cells differentiate into neurons and promote axon elongation in spinal cord slice cultures: their role in cell transplantation therapy for spinal cord injury. Neurorehabil Neural Repair 2008 22 : 447 457.
24. Yano S, Kuroda S, Lee JB et al. In vivo fluorescence tracking of bone marrow stromal cells transplanted into a pneumatic injury model of rat spinal cord. J Neurotrauma 2005 22 : 907 918.
25. Yano S, Kuroda S, Shichinohe H, Hida K, Iwasaki Y. Do bone marrow stromal cells proliferate after transplantation into mice cerebral infarct?-a double labeling study. Brain Res 2005 1065 : 60 67.
26. Yano S, Kuroda S, Shichinohe H et al. Bone marrow stromal cell transplantation preserves gammaaminobutyric acid receptor function in the injured spinal cord. J Neurotrauma 2006 23 : 1682 1692.
27. Cernak I, Vink R, Zapple DN et al. The pathobiology of moderate diffuse traumatic brain injury as identified using a new experimental model of injury in rats. Neurobiol Dis 2004 17 : 29 43.
28. Maruichi K, Kuroda S, Chiba Y et al. Graded model of diffuse axonal injury for studying head injury-induced cognitive dysfunction in rats. Neuropathology 2009 (in press).
29. Seki T, Hida K, Tada M, Koyanagi I, Iwasaki Y. Graded contusion model of the mouse spinal cord using a pneumatic impact device. Neurosurgery 2002 50 : 1075 1081 discussion 81 82.
30. Seki T, Hida K, Tada M, Koyanagi I, Iwasaki Y. Role of the bcl-2 gene after contusive spinal cord injury in mice. Neurosurgery 2003 53 : 192 198 discussion 98.
31. Lee JB, Kuroda S, Shichinohe H et al. Migration and differentiation of nuclear fluorescence-labeled bone marrow stromal cells after transplantation into cerebral infarct and spinal cord injury in mice. Neuropathology 2003 23 : 169 180.
32. Lee JB, Kuroda S, Shichinohe H et al. A pre-clinical assessment model of rat autogeneic bone marrow stromal cell transplantation into the central nervous system. Brain Res Brain Res Protoc 2004 14 : 37 44.
33. Shichinohe H, Kuroda S, Yano S, Hida K, Iwasaki Y. Role of SDF-1/CXCR4 system in survival and migration of bone marrow stromal cells after transplantation into mice cerebral infarct. Brain Res 2007 1138 : 138 147.
34. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 1984 11 : 47 60.
35. Sinson G, Voddi M, McIntosh TK. Combined fetal neural transplantation and nerve growth factor infusion: effects on neurological outcome following fluid-percussion brain injury in the rat. J Neurosurg 1996 84 : 655 662.
36. Philips MF, Mattiasson G, Wieloch T et al. Neuroprotective and behavioral efficacy of nerve growth factor-transfected hippocampal progenitor cell transplants after experimental traumatic brain injury. J Neurosurg 2001 94 : 765 774.
37. Watson DJ, Longhi L, Lee EB et al. Genetically modified NT2N human neuronal cells mediate long-term gene expression as CNS grafts in vivo and improve functional cognitive outcome following experimental traumatic brain injury. J Neuropathol Exp Neurol 2003 62 : 368 380.
38. Bakshi A, Shimizu S, Keck CA et al. Neural progenitor cells engineered to secrete GDNF show enhanced survival, neuronal differentiation and improve cognitive function following traumatic brain injury. Eur J Neurosci 2006 23 : 2119 2134.
39. Gao J, Prough DS, McAdoo DJ et al. Transplantation of primed human fetal neural stem cells improves cognitive function in rats after traumatic brain injury. Exp Neurol 2006 201 : 281 292.
40. Chen Y, Constantini S, Trembovler V, Weinstock M, Shohami E. An experimental model of closed head injury in mice: pathophysiology, histopathology, and cognitive deficits. J Neurotrauma 1996 13 : 557 568.
41. Pineda JA, Aono M, Sheng H et al. Extracellular superoxide dismutase overexpression improves behavioral outcome from closed head injury in the mouse. J Neurotrauma 2001 18 : 625 634.
42. Ding Y, Yao B, Lai Q, McAllister JP. Impaired motor learning and diffuse axonal damage in motor and visual systems of the rat following traumatic brain injury. Neurol Res 2001 23 : 193 202.
43. Sanchez-Ramos J, Song S, Cardozo-Pelaez F et al. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol 2000 164 : 247 256.
44. Woodbury D, Reynolds K, Black IB. Adult bone marrow stromal stem cells express germline, ectodermal, endodermal, and mesodermal genes prior to neurogenesis. J Neurosci Res 2002 69 : 908 917.
45. Yamaguchi S, Kuroda S, Kobayashi H et al. The effects of neuronal induction on gene expression profile in bone marrow stromal cells (BMSC)-a preliminary study using microarray analysis. Brain Res 2006 1087 : 15 27.
46. Kortesidis A, Zannettino A, Isenmann S, Shi S, Lapidot T, Gronthos S. Stromal-derived factor-1 promotes the growth, survival, and development of human bone marrow stromal stem cells. Blood 2005 105 : 3793 3801.
47. Gao Q, Li Y, Chopp M. Bone marrow stromal cells increase astrocyte survival via upregulation of phosphoinositide 3-kinase/threonine protein kinase and mitogen-activated protein kinase kinase/extracellular signal-regulated kinase pathways and stimulate astrocyte trophic factor gene expression after anaerobic insult. Neuroscience 2005 136 : 123 134.
48. Garcia R, Aguiar J, Alberti E, de la Cuetara K, Pavon N. Bone marrow stromal cells produce nerve growth factor and glial cell line-derived neurotrophic factors. Biochem Biophys Res Commun 2004 316 : 753 754.
49. Zhong C, Qin Z, Zhong CJ, Wang Y, Shen XY. Neuroprotective effects of bone marrow stromal cells on rat organotypic hippocampal slice culture model of cerebral ischemia. Neurosci Lett 2003 342 : 93 96.
50. Neuhuber B, Timothy Himes B, Shumsky JS, Gallo G, Fischer I. Axon growth and recovery of function supported by human bone marrow stromal cells in the injured spinal cord exhibit donor variations. Brain Res 2005 1035 : 73 85.
51. Chen X, Katakowski M, Li Y et al. Human bone marrow stromal cell cultures conditioned by traumatic brain tissue extracts: growth factor production. J Neurosci Res 2002 69 : 687 691. (Pubitemid 34966882)
52. Povlishock JT. Pathobiology of traumatically induced axonal injury in animals and man. Ann Emerg Med 1993 22 : 980 986.
53. Buki A, Povlishock JT. All roads lead to disconnection? - Traumatic axonal injury revisited. Acta Neurochir (Wien) 2006 148 : 181 193 discussion 93 94.
54. Pike BR, Zhao X, Newcomb JK, Glenn CC, Anderson DK, Hayes RL. Stretch injury causes calpain and caspase-3 activation and necrotic and apoptotic cell death in septo-hippocampal cell cultures. J Neurotrauma 2000 17 : 283 298.
55. Maxwell WL, McCreath BJ, Graham DI, Gennarelli TA. Cytochemical evidence for redistribution of membrane pump calcium-ATPase and ecto-Ca-ATPase activity, and calcium influx in myelinated nerve fibres of the optic nerve after stretch injury. J Neurocytol 1995 24 : 925 942.
56. Meythaler JM, Peduzzi JD, Eleftheriou E, Novack TA. Current concepts: diffuse axonal injury-associated traumatic brain injury. Arch Phys Med Rehabil 2001 82 : 1461 1471.
57. Alvarez-Dolado M, Pardal R, Garcia-Verdugo JM et al. Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 2003 425 : 968 973.
58. Terada N, Hamazaki T, Oka M et al. Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature 2002 416 : 542 545.