Suppression of neurocan and enhancement of axonal density in rats after treatment of traumatic brain injury with scaffolds impregnated with bone marrow stromal cells

Journal of Neurosurgery

Volumn 120, Issue 5, 2014, Pages 1147-1155

  Mahmood, Asim ^a   Wu, Hongtao ^a   Qu, Changsheng ^a   Mahmood, Selina ^a   Xiong, Y E ^a   Kaplan, David L ^c   Chopp, Michael ^a,b  

^a HENRY FORD HOSPITAL   (United States)

^b OAKLAND UNIVERSITY   (United States)

^c Tufts University   (United States)

Author keywords

Bone marrow stromal cells; Neurocan; Scaffolds; Traumatic brain injury

Indexed keywords

NEUROCAN; NEUROMODULIN; SYNAPTOPHYSIN; TISSUE SCAFFOLD;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BONE MARROW STROMAL CELL; BONE MARROW TRANSPLANTATION; BRAIN CORTEX LESION; BRAIN TISSUE; CELL DENSITY; COMPARATIVE STUDY; CONTROLLED STUDY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; LASER CAPTURE MICRODISSECTION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRAUMATIC BRAIN INJURY; TREATMENT DURATION; UPREGULATION;

ANIMALS; AXONS; BRAIN INJURIES; COLLAGEN; DISEASE MODELS, ANIMAL; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; NEUROCAN; RATS; RATS, WISTAR; RECOVERY OF FUNCTION; TISSUE SCAFFOLDS;

EID: 84899844045     PISSN: 00223085     EISSN: 19330693     Source Type: Journal    
DOI: 10.3171/2013.12.JNS131362     Document Type: Article

References (61)

1. Ahmed Z, Suggate EL, Brown ER, Dent RG, Armstrong SJ, Barrett LB, et al: Schwann cell-derived factor-induced modulation of the NgR/p75NTR/EGFR axis disinhibits axon growth through CNS myelin in vivo and in vitro. Brain 129:1517-1533, 2006 (Pubitemid 43999384)
2. Asher RA, Morgenstern DA, Fidler PS, Adcock KH, Oohira A, Braistead JE, et al: Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J Neurosci 20:2427-2438, 2000 (Pubitemid 30220330)
3. Asher RA, Morgenstern DA, Moon LD, Fawcett JW: Chondroitin sulphate proteoglycans: inhibitory components of the glial scar. Prog Brain Res 132:611-619, 2001
4. Aya-ay J, Mayer J, Eakin AK, Muffly BG, Anello M, Sandy JD, et al: The effect of hypoxic-ischemic brain injury in perinatal rats on the abundance and proteolysis of brevican and NG2. Exp Neurol 193:149-162, 2005 (Pubitemid 40463277)
5. Benfey M, Aguayo AJ: Extensive elongation of axons from rat brain into peripheral nerve grafts. Nature 296:150-152, 1982 (Pubitemid 12160909)
6. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, et al: Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416:636-640, 2002 (Pubitemid 34406764)
7. Bregman BS, Kunkel-Bagden E, Schnell L, Dai HN, Gao D, Schwab ME: Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature 378:498-501, 1995
8. Brösamle C, Huber AB, Fiedler M, Skerra A, Schwab ME: Regeneration of lesioned corticospinal tract fibers in the adult rat induced by a recombinant, humanized IN-1 antibody fragment. J Neurosci 20:8061-8068, 2000
9. Buchli AD, Schwab ME: Inhibition of Nogo: a key strategy to increase regeneration, plasticity and functional recovery of the lesioned central nervous system. Ann Med 37:556-567, 2005 (Pubitemid 41780144)
10. Cai D, Shen Y, De Bellard M, Tang S, Filbin MT: Prior exposure to neurotrophins blocks inhibition of axonal regeneration by MAG and myelin via a cAMP-dependent mechanism. Neuron 22:89-101, 1999 (Pubitemid 29070096)
11. Calza L, Giardino L, Giuliani A, Aloe L, Levi-Montalcini R: Nerve growth factor control of neuronal expression of angiogenetic and vasoactive factors. Proc Natl Acad Sci U S A 98: 4160-4165, 2001 (Pubitemid 32249915)
12. Carmichael ST, Archibeque I, Luke L, Nolan T, Momiy J, Li S: Growth-associated gene expression after stroke: evidence for a growth-promoting region in peri-infarct cortex. Exp Neurol 193:291-311, 2005 (Pubitemid 40616180)
13. Caroni P, Schwab ME: Antibody against myelin-associated inhibitor of neurite growth neutralizes nonpermissive substrate properties of CNS white matter. Neuron 1:85-96, 1988
14. Chen J, Zhang ZG, Li Y, Wang Y, Wang L, Jiang H, et al: Statins induce angiogenesis, neurogenesis, and synaptogenesis after stroke. Ann Neurol 53:743-751, 2003 (Pubitemid 36622511)
15. Chen X, Katakowski M, Li Y, Lu D, Wang L, Zhang L, et al: Human bone marrow stromal cell cultures conditioned by traumatic brain tissue extracts: growth factor production. J Neurosci Res 69:687-691, 2002 (Pubitemid 34966882)
16. Chytrova G, Ying Z, Gomez-Pinilla F: Exercise normalizes levels of MAG and Nogo-A growth inhibitors after brain trauma. Eur J Neurosci 27:1-11, 2008
17. Davies SJ, Field PM, Raisman G: Regeneration of cut adult axons fails even in the presence of continuous aligned glial pathways. Exp Neurol 142:203-216, 1996 (Pubitemid 26414055)
18. Davies SJ, Goucher DR, Doller C, Silver J: Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J Neurosci 19:5810-5822, 1999 (Pubitemid 29327918)
19. Deguchi K, Takaishi M, Hayashi T, Oohira A, Nagotani S, Li F, et al: Expression of neurocan after transient middle cerebral artery occlusion in adult rat brain. Brain Res 1037:194-199, 2005 (Pubitemid 40362396)
20. Dixon CE, Clifton GL, Lighthall JW, Yaghmai AA, Hayes RL: A controlled cortical impact model of traumatic brain injury in the rat. J Neurosci Methods 39:253-262, 1991
21. Fidler PS, Schuette K, Asher RA, Dobbertin A, Thornton SR, Calle-Patino Y, et al: Comparing astrocytic cell lines that are inhibitory or permissive for axon growth: the major axon-inhibitory proteoglycan is NG2. J Neurosci 19:8778-8788, 1999 (Pubitemid 30226699)
22. Harris NG, Carmichael ST, Hovda DA, Sutton RL: Traumatic brain injury results in disparate regions of chondroitin sulfate proteoglycan expression that are temporally limited. J Neurosci Res 87:2937-2950, 2009
23. Hulsebosch CE, DeWitt DS, Jenkins LW, Prough DS: Traumatic brain injury in rats results in increased expression of Gap-43 that correlates with behavioral recovery. Neurosci Lett 255:83-86, 1998 (Pubitemid 28494204)
24. Katoh-Semba R, Matsuda M, Watanabe E, Maeda N, Oohira A: Two types of brain chondroitin sulfate proteoglycan: their distribution and possible functions in the rat embryo. Neurosci Res 31:273-282, 1998 (Pubitemid 28446010)
25. Katsman D, Zheng J, Spinelli K, Carmichael ST: Tissue microenvironments within functional cortical subdivisions adjacent to focal stroke. J Cereb Blood Flow Metab 23:997-1009, 2003 (Pubitemid 37082425)
26. Lee DH, Strittmatter SM, Sah DW: Targeting the Nogo receptor to treat central nervous system injuries. Nat Rev Drug Discov 2:872-878, 2003 (Pubitemid 37407793)
27. Lee JK, Kim JE, Sivula M, Strittmatter SM: Nogo receptor antagonism promotes stroke recovery by enhancing axonal plasticity. J Neurosci 24:6209-6217, 2004 (Pubitemid 38891112)
28. Lemons ML, Howland DR, Anderson DK: Chondroitin sulfate proteoglycan immunoreactivity increases following spinal cord injury and transplantation. Exp Neurol 160:51-65, 1999
29. Lenzlinger PM, Shimizu S, Marklund N, Thompson HJ, Schwab ME, Saatman KE, et al: Delayed inhibition of Nogo-A does not alter injury-induced axonal sprouting but enhances recovery of cognitive function following experimental traumatic brain injury in rats. Neuroscience 134:1047-1056, 2005 (Pubitemid 41133405)
30. Li Y, Chen J, Zhang CL, Wang L, Lu D, Katakowski M, et al: Gliosis and brain remodeling after treatment of stroke in rats with marrow stromal cells. Glia 49:407-417, 2005 (Pubitemid 40222918)
31. Liu Z, Li Y, Qu R, Shen L, Gao Q, Zhang X, et al: 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 1149:172-180, 2007 (Pubitemid 46659890)
32. 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 18:813-819, 2001 (Pubitemid 32769777)
33. Lu D, Mahmood A, Chopp M: Biologic transplantation and neurotrophin-induced neuroplasticity after traumatic brain injury. J Head Trauma Rehabil 18:357-376, 2003 (Pubitemid 36899046)
34. 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 61:596-603, 2007
35. 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 12:559-563, 2001 (Pubitemid 32173965)
36. Mahmood A, Lu D, Chopp M: Intravenous administration of marrow stromal cells (MSCs) increases the expression of growth factors in rat brain after traumatic brain injury. J Neurotrauma 21:33-39, 2004 (Pubitemid 38141800)
37. 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 53:697-703, 2003 (Pubitemid 37055948)
38. 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 57:1026-1031, 2005
39. 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 19:1609-1617, 2002 (Pubitemid 36026216)
40. 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 49:1196-1204, 2001 (Pubitemid 32995857)
41. Mahmood A, Lu D, Yi L, Chen JL, Chopp M: Intracranial bone marrow transplantation after traumatic brain injury improving functional outcome in adult rats. J Neurosurg 94:589-595, 2001 (Pubitemid 32799652)
42. Mahmood A, Wu H, Qu C, Xiong Y, Chopp M: Effects of treating traumatic brain injury with collagen scaffolds and human bone marrow stromal cells on sprouting of corticospinal tract axons into the denervated side of the spinal cord. Laboratory investigation. J Neurosurg 118:381-389, 2013
43. Margolis RK, Rauch U, Maurel P, Margolis RU: Neurocan and phosphacan: two major nervous tissue-specific chondroitin sulfate proteoglycans. Perspect Dev Neurobiol 3:273-290, 1996 (Pubitemid 126839136)
44. Marklund N, Bareyre FM, Royo NC, Thompson HJ, Mir AK, Grady MS, et al: Cognitive outcome following brain injury and treatment with an inhibitor of Nogo-A in association with an attenuated downregulation of hippocampal growth-associated protein-43 expression. J Neurosurg 107:844-853, 2007 (Pubitemid 47547752)
45. Matsui F, Kawashima S, Shuo T, Yamauchi S, Tokita Y, Aono S, et al: Transient expression of juvenile-type neurocan by reactive astrocytes in adult rat brains injured by kainate-induced seizures as well as surgical incision. Neuroscience 112:773-781, 2002 (Pubitemid 34667042)
46. Matsui F, Watanabe E, Oohira A: Immunological identification of two proteoglycan fragments derived from neurocan, a brain-specific chondroitin sulfate proteoglycan. Neurochem Int 25:425-431, 1994
47. McKeon RJ, Höke A, Silver J: Injury-induced proteoglycans inhibit the potential for laminin-mediated axon growth on astrocytic scars. Exp Neurol 136:32-43, 1995
48. Moon LD, Asher RA, Rhodes KE, Fawcett JW: Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nat Neurosci 4:465-466, 2001 (Pubitemid 32397182)
49. Moon LD, Asher RA, Rhodes KE, Fawcett JW: Relationship between sprouting axons, proteoglycans and glial cells following unilateral nigrostriatal axotomy in the adult rat. Neuroscience 109:101-117, 2002 (Pubitemid 34088150)
50. Papadopoulos CM, Tsai SY, Alsbiei T, O'Brien TE, Schwab ME, Kartje GL: Functional recovery and neuroanatomical plasticity following middle cerebral artery occlusion and IN-1 antibody treatment in the adult rat. Ann Neurol 51:433-441, 2002 (Pubitemid 34260773)
51. Posmantur R, Kampfl A, Siman R, Liu J, Zhao X, Clifton GL, et al: A calpain inhibitor attenuates cortical cytoskeletal protein loss after experimental traumatic brain injury in the rat. Neuroscience 77:875-888, 1997 (Pubitemid 27092142)
52. Qu C, Mahmood A, Liu XS, Xiong Y, Wang L, Wu H, et al: The treatment of TBI with human marrow stromal cells impregnated into collagen scaffold: functional outcome and gene expression profile. Brain Res 1371:129-139, 2011
53. Schnell L, Schwab ME: Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 343:269-272, 1990 (Pubitemid 20030644)
54. Shen LH, Li Y, Gao Q, Savant-Bhonsale S, Chopp M: Downregulation of neurocan expression in reactive astrocytes promotes axonal regeneration and facilitates the neurorestorative effects of bone marrow stromal cells in the ischemic rat brain. Glia 56:1747-1754, 2008
55. Thompson HJ, Marklund N, LeBold DG, Morales DM, Keck CA, Vinson M, et al: Tissue sparing and functional recovery following experimental traumatic brain injury is provided by treatment with an anti-myelin-associated glycoprotein antibody. Eur J Neurosci 24:3063-3072, 2006 (Pubitemid 44952638)
56. Vitkoviæ L, Steisslinger HW, Aloyo VJ, Mersel M: The 43-kDa neuronal growth-associated protein (GAP-43) is present in plasma membranes of rat astrocytes. Proc Natl Acad Sci U S A 85:8296-8300, 1988
57. Watanabe E, Aono S, Matsui F, Yamada Y, Naruse I, Oohira A: Distribution of a brain-specific proteoglycan, neurocan, and the corresponding mRNA during the formation of barrels in the rat somatosensory cortex. Eur J Neurosci 7:547-554, 1995
58. Wiessner C, Bareyre FM, Allegrini PR, Mir AK, Frentzel S, Zurini M, et al: Anti-Nogo-A antibody infusion 24 hours after experimental stroke improved behavioral outcome and corticospinal plasticity in normotensive and spontaneously hypertensive rats. J Cereb Blood Flow Metab 23:154-165, 2003 (Pubitemid 36188454)
59. Wright KT, El Masri W, Osman A, Roberts S, Chamberlain G, Ashton BA, et al: Bone marrow stromal cells stimulate neurite outgrowth over neural proteoglycans (CSPG), myelin associated glycoprotein and Nogo-A. Biochem Biophys Res Commun 354:559-566, 2007 (Pubitemid 46161360)
60. Xiong Y, Qu C, Mahmood A, Liu Z, Ning R, Li Y, et al: 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 Res 1263:183-191, 2009
61. Yiu G, He Z: Glial inhibition of CNS axon regeneration. Nat Rev Neurosci 7:617-627, 2006 (Pubitemid 44106744)