Combinatory treatments needed for spinal cord injury

Experimental Neurology

Volumn 248, Issue , 2013, Pages 309-315

  Olson, Lars ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 1; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GROWTH FACTOR; IMATINIB; MYELIN; N ACETYLGALACTOSAMINE 4 SULFATASE; NEUROTROPHIN; PROTEIN NOGO A; PROTEOCHONDROITIN SULFATE; ROLIPRAM;

GRAY MATTER; HUMAN; NEOPLASM; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVE FIBER REGENERATION; NERVE GRAFT; NERVE GROWTH; NERVE SPROUTING; NEURAL STEM CELL; NEUROPROTECTION; NEUROTROPISM; NONHUMAN; NOTE; PRIORITY JOURNAL; PYRAMIDAL TRACT; SCHWANN CELL; SENSORY NERVE; SPINAL CORD INJURY; WHITE MATTER;

ANIMALS; COMBINED MODALITY THERAPY; DISEASE MODELS, ANIMAL; HUMANS; SPINAL CORD INJURIES;

EID: 84880842854     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.06.024     Document Type: Note

References (97)

1. Abrams M.B., Nilsson I., Lewandowski S., Codeluppi S., Olson L., Eriksson U. Imatinib enhances functional outcome after spinal cord injury. PLoS One 2012, 7(6). (e38760).
2. Akbik F., Cafferty W.B., Strittmatter S.M. Myelin associated inhibitors: a link between injury-induced and experience-dependent plasticity. Exp. Neurol. 2012, 235:43-52.
3. Atwal J.K., Pinkston-Gosse J., Syken J., Stawicki S., Wu Y., Shatz C., Tessier-Lavigne M. PirB is a functional receptor for myelin inhibitors of axonal regeneration. Science 2008, 322:967-970.
4. Barthélemy D., Alain S., Grey M., Nielsen J., Bouyer L. Rapid changes in corticospinal excitability during force field adaptation of human walking. Exp. Brain Res. 2012, 217:99-115.
5. Berry M. Post-injury myelin-breakdown products inhibit axonal growth: an hypothesis to explain the failure of axonal regeneration in the mammalian central nervous system. Bibl. Anat. 1982, 23:1-11.
6. Blesch A., Lu P., Tuszynski M.H. Neurotrophic factors, gene therapy, and neural stem cells for spinal cord repair. Brain Res. Bull. 2002, 57:833-838.
7. Borrie S.C., Baeumer B.E., Bandtlow C.E. The Nogo-66 receptor family in the intact and diseased CNS. Cell Tissue Res. 2012, 349:105-117.
8. Bradbury E.J., Moon L.D., Popat R.J., King V.R., Bennett G.S., Patel P.N., Fawcett J.W. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002, 416:636-640.
9. Bunge R.P., Puckett W.R., Becerra J.L., Marcillo A., Quencer R.M. Observations on the pathology of human spinal cord injury. A review and classification of 22 new cases with details from a case of chronic cord compression with extensive focal demyelination. Adv. Neurol. 1993, 59:75-89.
10. Cafferty W.B., Duffy P., Huebner E., Strittmatter S.M. MAG and OMgp synergize with Nogo-A to restrict axonal growth and neurological recovery after spinal cord trauma. J. Neurosci. 2010, 30:6825-6837.
11. Caroni P., Schwab M.E. Two membrane protein fractions from rat central myelin with inhibitory properties for neurite growth and fibroblast spreading. J. Cell Biol. 1988, 106:1281-1288.
12. Caroni P., Schwab M.E. Antibody against myelin-associated inhibitor of neurite growth neutralizes nonpermissive substrate properties of CNS white matter. Neuron 1988, 1:85-96.
13. Casha, McGowan D., Bains I., Yong W., Hurlbert R. Results of a phase II placebo-controlled randomized trial of minocycline in acute spinal cord injury. Brain 2012, 135:1224-1236.
14. Castermans T., Duvinage M. Corticomuscular coherence revealed during treadmill walking: further evidence of supraspinal control in human locomotion. J. Physiol. 2013, 591:1407-1408.
15. Chen M.S., Huber A.B., van der Haar M.E., Frank M., Schnell L., Spillmann A.A., Christ F., Schwab M.E. Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 2000, 403:434-439.
16. Cheng H., Cao Y., Olson L. Spinal cord repair in adult paraplegic rats: partial restoration of hind limb function. Science 1996, 273:510-513.
17. Cheng H., Almström S., Giménez-Llort L., Chang R., Ögren S.O., Hoffer B., Olson L. Gait analysis of adult paraplegic rats after spinal cord repair. Exp. Neurol. 1997, 148:544-557.
18. Cheng H., Fraidakis M., Blombäck B., Lapchak P., Hoffer B., Olson L. Characterization of a fibrin glue-GDNF slow-release preparation. Cell Transplant. 1998, 7:53-61.
19. Chong S.Y., Rosenberg S.S., Fancy S.P., Zhao C., Shen Y.A., Hahn A.T., McGee A.W., Xu X., Zheng B., Zhang L.I., Rowitch D.H., Franklin R.J., Lu Q.R., Chan J.R. Neurite outgrowth inhibitor Nogo-A establishes spatial segregation and extent of oligodendrocyte myelination. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:1299-1304.
20. Davies S., Fitch M., Memberg S., Hall A., Raisman G., Silver J. Regeneration of adult axons in white matter tracts of the central nervous system. Nature 1997, 390:680-683.
21. Davies S., Goucher D., Doller C., Silver J. Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J. Neurosci. 1999, 19:5810-5822.
22. Deng L.X., Deng P., Ruan Y., Xu Z.C., Liu N.K., Wen X., Smith G.M., Xu X.M. A novel growth-promoting pathway formed by GDNF-overexpressing Schwann cells promotes propriospinal axonal regeneration, synapse formation, and partial recovery of function after spinal cord injury. J. Neurosci. 2013, 33:5655-5667.
23. Dickendesher T.L., Baldwin K.T., Mironova Y.A., Koriyama Y., Raiker S.J., Askew K.L., Wood A., Geoffroy C.G., Zheng B., Liepmann C.D., Katagiri Y., Benowitz L.I., Geller H.M., Giger R.J. NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nat. Neurosci. 2012, 15:703-712.
24. Endo T., Spenger C., Tominaga T., Brené S., Olson L. Cortical sensory map rearrangement after spinal cord injury: fMRI responses linked to Nogo signalling. Brain 2007, 130:2951-2961.
25. Fehlings M., Theodore N., Harrop J., Maurais G., Charles Kuntz C., Shaffrey C., Kwon B., Chapman J., Albert Yee A., Tighe A., McKerracher L. A phase I/IIa clinical trial of a recombinant Rho protein antagonist in acute spinal cord injury. J. Neurotrauma 2011, 28:787-796.
26. Filli L., Schwab M.E. The rocky road to translation in spinal cord repair. Ann. Neurol. 2012, 72:491-501.
27. Fischer D., He Z., Benowitz L.I. Counteracting the Nogo receptor enhances optic nerve regeneration if retinal ganglion cells are in an active growth state. J. Neurosci. 2004, 24:1646-1651.
28. Flora G., Joseph G., Patel S., Singh A., Bleicher D., Barakat D.J., Louro J., Fenton S., Garg M., Bunge M.B., Pearse D.D. Combining neurotrophin transduced Schwann cells and rolipram to promote functional recovery from spinal cord injury. Cell Transplant. 2012, (Nov 8. [Epub ahead of print]).
29. Fortun J., Hill C.E., Bunge M.B. Combinatorial strategies with Schwann cell transplantation to improve repair of the injured spinal cord. Neurosci. Lett. 2009, 456:124-132.
30. Fournier A.E., GrandPre T., Strittmatter S.M. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 2001, 409:341-346.
31. Fournier A.E., Gould G.C., Liu B.P., Strittmatter S.M. Truncated soluble Nogo receptor binds Nogo-66 and blocks inhibition of axon growth by myelin. J. Neurosci. 2002, 22:8876-8883.
32. Fraidakis M.J. Lugaro's forgotten legacy: the hypothesis of negative neurotropism. J. Hist. Neurosci. 2010, 19:239-252.
33. Fraidakis M.J., Spenger L., Olson L. Partial recovery after treatment of chronic paraplegia in rat. Exp. Neurol. 2004, 188:33-42.
34. García-Alías G., Fawcett J.W. Training and anti-CSPG combination therapy for spinal cord injury. Exp. Neurol. 2012, 235:26-32.
35. García-Alías G., Petrosyan H.A., Schnell L., Horner P.J., Bowers W.J., Mendell L.M., Fawcett J.W., Arvanian V.L. Chondroitinase ABC combined with neurotrophin NT-3 secretion and NR2D expression promotes axonal plasticity and functional recovery in rats with lateral hemisection of the spinal cord. J. Neurosci. 2011, 31:17788-17799.
36. Gensel J.C., Donnelly D.J., Popovich P.G. Spinal cord injury therapies in humans: an overview of current clinical trials and their potential effects on intrinsic CNS macrophages. Expert. Opin. Ther. Targets 2011, 15:505-518.
37. GrandPre T., Nakamura F., Vartanian T., Strittmatter S.M. Identification of the Nogo inhibitor of axon regeneration as a Reticulon protein. Nature 2000, 403:439-444.
38. Hiraoka K., Abe K. Cortical and spinal control of ankle joint muscles before and during gait initiation. Somatosens. Mot. Res. 2007, 24:127-133.
39. Hofstetter C.P., Holmström N.A., Lilja J.A., Schweinhardt P., Hao J., Spenger C., Wiesenfeld-Hallin Z., Kurpad S.N., Frisen J., Olson L. Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat. Neurosci. 2005, 8:346-353.
40. Jain S., Gourab K., Schindler-Ivens S., Schmit B.D. EEG during pedaling: evidence for cortical control of locomotor tasks. Clin. Neurophysiol. 2013, 124:379-390.
41. Josephson A., Greitz D., Klason T., Olson L., Spenger C. A spinal thecal sac constriction model supports the theory that induced pressure gradients in the cord cause edema and cyst formation. Neurosurgery 2001, 48:636-645. (discussion 645?636).
42. Josephson A., Widenfalk J., Widmer H.W., Olson L., Spenger C. NOGO mRNA expression in adult and fetal human and rat nervous tissue and in weight drop injury. Exp. Neurol. 2001, 169:319-328.
43. Josephson A., Trifunovski A., Widmer H.R., Widenfalk J., Olson L., Spenger C. Nogo-receptor gene activity: cellular localization and developmental regulation of mRNA in mice and humans. J. Comp. Neurol. 2002, 453:292-304.
44. Josephson A., Trifunovski A., Scheele C., Widenfalk J., Wahlestedt C., Brene S., Olson L., Spenger C. Activity-induced and developmental downregulation of the Nogo receptor. Cell Tissue Res. 2003, 311:333-342.
45. Karimi-Abdolrezaee S., Eftekharpour E., Wang J., Schut D., Fehlings M.G. Synergistic effects of transplanted adult neural stem/progenitor cells, chondroitinase, and growth factors promote functional repair and plasticity of the chronically injured spinal cord. J. Neurosci. 2010, 30:1657-1676.
46. Karlén A., Karlsson T.E., Mattsson A., Lundströmer K., Pham T.M., Bäckman C.M., Ögren S.O., Hoffman A.F., Sherling M.A., Lupica C.R., Hoffer B.J., Spenger C., Josephson A., Brené S., Olson L. Nogo receptor 1 regulates formation of lasting memories. PNAS 2009, 106:20476-20481.
47. Karlsson T.E., Koczy J., Brené S., Olson L., Josephson A. Differential conserted activity induced regulation of Nogo receptors (1?3), LOTUS and Nogo mRNA in mouse brain. PLoS One 2013, 8:e60892.
48. Kopp M.A., Liebscher T., Niedeggen A., Laufer S., Brommer B., Jungehulsing G.J., Strittmatter S.M., Dirnagl U., Schwab J.M. Small-molecule-induced Rho-inhibition: NSAIDs after spinal cord injury. Cell Tissue Res. 2012, 349:119-132.
49. Kwon B.K., Tetzlaff W. Spinal cord regeneration: from gene to transplants. Spine 2001, 26(24 Suppl):S13-S22.
50. Lauren J., Airaksinen M.S., Saarma M., Timmusk T. Two novel mammalian Nogo receptor homologs differentially expressed in the central and peripheral nervous systems. Mol. Cell. Neurosci. 2003, 24:581-594.
51. Lauren J., Hu F., Chin J., Liao J., Airaksinen M.S., Strittmatter S.M. Characterization of myelin ligand complexes with neuronal Nogo-66 receptor family members. J. Biol. Chem. 2007, 282:5715-5725.
52. Le Gros Clark W.E. The problem of neuronal regeneration in the central nervous system. I. The influence of spinal ganglia and nerve fragments grafted in the brain. J. Anat. 1943, 77:29-48.
53. Lee Y.S., Hsiao I., Lin V.W. Peripheral nerve grafts and aFGF restore partial hindlimb function in adult paraplegic rats. J. Neurotrauma 2002, 19:1203-1216.
54. Lee Y.S., Lin C.Y., Robertson R.T., Hsiao I., Lin V.W. Motor recovery and anatomical evidence of axonal regrowth in spinal cord-repaired adult rats. J. Neuropathol. Exp. Neurol. 2004, 63:233-245.
55. Lee Y.S., Zdunowski S., Edgerton V.R., Roy R.R., Zhong H., Hsiao I., Lin V.W. Improvement of gait patterns in step-trained, complete spinal cord-transected rats treated with a peripheral nerve graft and acidic fibroblast growth factor. Exp. Neurol. 2010, 224:429-437.
56. Lee Y.S., Lin C.Y., Jiang H.H., Depaul M., Lin V.W., Silver J. Nerve regeneration restores supraspinal control of bladder function after complete spinal cord injury. J. Neurosci. 2013, 33:10591-10606.
57. Liebscher T., Schnell L., Schnell D., Scholl J., Schneider R., Gullo M., Fouad K., Mir A., Rausch M., Kindler D., Hamers F.P., Schwab M.E. Nogo-A antibody improves regeneration and locomotion of spinal cord-injured rats. Ann. Neurol. 2005, 58:706-719.
58. Lu P., Wang Y., Graham L., McHale K., Gao M., Wu D., Brock J., Blesch A., Rosenzweig E.S., Havton L.A., Zheng B., Conner J.M., Marsala M., Tuszynski M.H. Long-distance growth and connectivity of neural stem cells after severe spinal cord injury. Cell 2012, 150:1264-1273.
59. Madhavan S., Krishnan C., Jayaraman A., Rymer W.Z., Stinear J.W. Corticospinal tract integrity correlates with knee extensor weakness in chronic stroke survivors. Clin. Neurophysiol. 2011, 122:1588-1594.
60. Maier I.C., Ichiyama R.M., Courtine G., Schnell L., Lavrov I., Edgerton V.R., Schwab M.E. Differential effects of anti-Nogo-A antibody treatment and treadmill training in rats with incomplete spinal cord injury. Brain 2009, 132:1426-1440.
61. Marinesco G. Recherhes sur la régénérescence de la moelle. Nouvelle Iconographie de la Salpêtrière 1906, 5.
62. McGee A.W., Yang Y., Fischer Q.S., Daw N.W., Strittmatter S.M. Experience-driven plasticity of visual cortex limited by myelin and Nogo receptor. Science 2005, 132:2222-2226.
63. McKerracher L., David S., Jackson D.L., Kottis V., Dunn R.J., Braun P.E. Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 1994, 13:805-811.
64. Mi S., Lee X., Shao Z., Thill G., Ji B., Relton J., Levesque M., Allaire N., Perrin S., Sands B., Crowell T., Cate R.L., McCoy J.M., Pepinsky R.B. LINGO-1 is a component of the Nogo-66 receptor/p75 signaling complex. Nat. Neurosci. 2004, 7:221-228.
65. Morgenstern D.A., Asher R.A., Fawcett J.W. Chondroitin sulphate proteoglycans in the CNS injury response. Prog. Brain Res. 2002, 137:313-332.
66. Mukhopadhyay G., Doherty P., Walsh F.S., Crocker P.R., Filbin M.T. A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 1994, 13:757-767.
67. Nielsen J.B. Motoneuronal drive during human walking. Brain Res. Rev. 2002, 40:192-201.
68. Nielsen J.B. How we walk: central control of muscle activity during human walking. Neuroscientist 2003, 9:195-204.
69. Nygren L.-G., Olson L., Seiger Å. Regeneration of monoamine-containing axons in the developing and adult spinal cord of the rat following intraspinal 6-OH-dopamine injections or transections. Histochemie 1971, 28:1-15.
70. Olson L. Intact and regenerating sympathetic noradrenaline axons in the rat sciatic nerve. Histochemie 1969, 17:349-367.
71. Olson L. Regeneration in the central nervous system. Nat. Med. 1997, 3:1329-1335.
72. Park J.B., Yiu G., Kaneko S., Wang J., Chang J., He X.L., Garcia K.C., He Z. A TNF receptor family member, TROY, is a coreceptor with Nogo receptor in mediating the inhibitory activity of myelin inhibitors. Neuron 2005, 45:345-351.
73. Pernet V., Schwab M.E. The role of Nogo-A in axonal plasticity, regrowth and repair. Cell Tissue Res. 2012, 349:97-104.
74. Petersen N., Pyndt H., Nielsen J. Investigating human motor control by transcranial magnetic stimulation. Exp. Brain Res. 2003, 152:1-16.
75. Petersen J., Martina Spies M., Curt A., Dietz V., Schubert M., EM-SCI Study Group Spinal cord injury: one-year evolution of motor-evoked potentials and recovery of leg motor function in 255 patients. Neurorehab and Neural Repair 2012, 26:939-948.
76. Petersen T., Willerslev-Olsen M., Conway B., Nielsen J. The motor cortex drives the muscles during walking in human subjects. J. Physiol. 2012, 590:2443-2452.
77. Popovich P.G. Building bridges for spinal cord repair. Cell 2012, 150:1105-1106.
78. Prinjha R., Moore S.E., Vinson M., Blake S., Morrow R., Christie G., Michalovich D., Simmons D.L., Walsh F.S. Inhibitor of neurite outgrowth in humans. Nature 2000, 403:383-384.
79. Ram ón y Cajal S. Degeneration and Regeneration in the Nervous System 1928, (and transl), Humphrey Milford and Oxford University Press, London. R.M. May (Ed.).
80. Richardson P.M., McGuiness U.M., Aguayo A.J. Axons from CNS neurons regenerate into PNS grafts. Nature 1980, 284:264-265.
81. Sahni V., Kessler J.A. Stem cell therapies for spinal cord injury. Nat. Rev. Neurol. 2010, 6:363-372.
82. Sahyoun C., Floyer-Lea A., Johansen-Berg H., Matthews P. Towards an understanding of gait control: brain activation during the anticipation, preparation and execution of foot movements. NeuroImage 2004, 21:568-575.
83. Sato Y., Iketani M., Kurihara Y., Yamaguchi M., Yamashita N., Nakamura F., Arie Y., Kawasaki T., Hirata T., Abe T., Kiyonari H., Strittmatter S.M., Goshima Y., Takei K. Cartilage acidic protein-1B (LOTUS), an endogenous Nogo receptor antagonist for axon tract formation. Science 2011, 333:769-773.
84. Schwab M.E. Functions of Nogo proteins and their receptors in the nervous system. Nat. Rev. Neurosci. 2010, 11:799-811.
85. Shao Z., Browning J.L., Lee X., Scott M.L., Shulga-Morskaya S., Allaire N., Thill G., Levesque M., Sah D., McCoy J.M., Murray B., Jung V., Pepinsky R.B., Mi S. TAJ/TROY, an orphan TNF receptor family member, binds Nogo-66 receptor 1 and regulates axonal regeneration. Neuron 2005, 45:353-359.
86. Sharma K., Selzer M.E., Li S. Scar-mediated inhibition and CSPG receptors in the CNS. Exp. Neurol. 2012, 237:370-378.
87. Starkey M.L., Bartus K., Barritt A.W., Bradbury E.J. Chondroitinase ABC promotes compensatory sprouting of the intact corticospinal tract and recovery of forelimb function following unilateral pyramidotomy in adult mice. Eur. J. Neurosci. 2012, 36:3665-3678.
88. Syken J., Grandpre T., Kanold P.O., Shatz C.J. PirB restricts ocular-dominance plasticity in visual cortex. Science 2006, 313:1795-1800.
89. Tabakow P., Jarmundowicz W., Czapiga B., Fortuna W., Miedzybrodzki R., Czyz M., Huber J., Szarek D., Okurowski S., Szewczyk P., Gorski A., Raisman G. Transplantation of autologous olfactory ensheathing cells in complete human spinal cord injury. Cell Transplant. 2013, (in press).
90. Tello F. La influencia del neurotropismo en la regeneraci ón de los centros nerviosos 1911, 9(Trab. Lab. Invest. Biol. Univ. Madrid):123-159.
91. Tom V.J., Sandrow-Feinberg H.R., Miller K., Domitrovich C., Bouyer J., Zhukareva V., Klaw M.C., Lemay M.A., Houlé J.D. Exogenous BDNF enhances the integration of chronically injured axons that regenerate through a peripheral nerve grafted into a chondroitinase-treated spinal cord injury site. Exp. Neurol. 2013, 239:91-100.
92. Tsai E., Krassioukov A.V., Tator C.H. Corticospinal regeneration into lumbar grey matter correlates with locomotor recovery after complete spinal cord transection and repair with peripheral nerve grafts, fibroblast growth factor 1, fibrin glue, and spinal fusion. J. Neuropathol. Exp. Neurol. 2005, 64:230-244.
93. Tsai S.Y., Papadopoulos C.M., Schwab M.E., Kartje G.L. Delayed anti-nogo-a therapy improves function after chronic stroke in adult rats. Stroke 2011, 42:186-190.
94. Wang K.C., Kim J.A., Sivasankaran R., Segal R., He Z. P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 2002, 420:74-78.
95. Wang K.C., Koprivica V., Kim J.A., Sivasankaran R., Guo Y., Neve R.L., He Z. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 2002, 417:941-944.
96. Wang X., Hasan O., Arzeno A., Benowitz L.I., Cafferty W.B., Strittmatter S.M. Axonal regeneration induced by blockade of glial inhibitors coupled with activation of intrinsic neuronal growth pathways. Exp. Neurol. 2012, 237:55-69.
97. Widenfalk J., Lundströmer K., Jubran M., Brené S., Olson L. Neurotrophic factors and receptors in the immature and adult spinal cord after mechanical injury or kainic acid. J. Neurosci. 2001, 21:3457-3475.