Invasion of lesion territory by regenerating fibers after spinal cord injury in adult macaque monkeys

Neuroscience

Volumn 227, Issue , 2012, Pages 271-282

  Beaud, M L ^a   Rouiller, E M ^a   Bloch, J ^c   Mir, A ^d   Schwab, M E ^b   Wannier, T ^a,b   Schmidlin, E ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

^b University of Zurich Brain Research Institute   (Switzerland)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^d NOVARTIS PHARMA AG   (Switzerland)

Author keywords

BDNF; Nogo A; Primate; Regeneration; Scar tissue; Spinal cord lesion

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; NOGO A ANTIBODY;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CONTROLLED STUDY; FEMALE; MALE; MOTONEURON; NERVE CELL GROWTH; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RHESUS MONKEY; SPINAL CORD INJURY; SPINAL CORD LESION;

ANIMALS; ANTIBODIES; BRAIN-DERIVED NEUROTROPHIC FACTOR; CHONDROITIN SULFATE PROTEOGLYCANS; DISEASE MODELS, ANIMAL; FEMALE; INJECTIONS, SPINAL; MACACA; MALE; MYELIN PROTEINS; NERVE FIBERS; NERVE REGENERATION; NEUROFILAMENT PROTEINS; RECOVERY OF FUNCTION; SPINAL CORD INJURIES;

EID: 84868331049     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.09.052     Document Type: Article

References (54)

1. Beaud M.L., Schmidlin E., Wannier T., Freund P., Bloch J., Mir A., Schwab M.E., Rouiller E.M. Anti-Nogo-A antibody treatment does not prevent cell body shrinkage in the motor cortex in adult monkeys subjected to unilateral cervical cord lesion. BMC Neurosci 2008, 9:5.
2. Bregman B.S., Kunkel-Bagden E., Schnell L., Dai H.N., Gao D., Schwab M.E. Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature 1995, 378:498-501.
3. Brook G.A., Plate D., Franzen R., Martin D., Moonen G., Schoenen J., Schmitt A.B., Noth J., Nacimiento W. Spontaneous longitudinally orientated axonal regeneration is associated with the Schwann cell framework within the lesion site following spinal cord compression injury of the rat. J Neurosci Res 1998, 53:51-65.
4. Brown J.O., MacCouch G.P. Abortive regeneration of the transected spinal cord. J Comp Neurol 1947, 87:131-137.
5. Campbell M.J., Morrison J.H. Monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex. J Comp Neurol 1989, 282:191-205.
6. Carriedo S.G., Yin H.Z., Weiss J.H. Motor neurons are selectively vulnerable to AMPA/kainate receptor-mediated injury in vitro. J Neurosci 1996, 16:4069-4079.
7. Clemente C.D. Structural regeneration of neuroglia and connective tissue. Regeneration in the central nervous system 1955, 147-161. Charles C. Thomas, Springfield. W.F. Windle (Ed.).
8. David S., Lacroix S. Molecular approaches to spinal cord repair. Annu Rev Neurosci 2003, 26:411-440.
9. Davies S.J., Fitch M.T., Memberg S.P., Hall A.K., Raisman G., Silver J. Regeneration of axons in white tracts of the central nervous system. Nature 1997, 390:680-683.
10. Davies S.J.A., Goucher D.R., 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.
11. De Castro R., Tajrishi R., Claros J., Stallcup W.B. Differential responses of spinal axons to transection: influence of the NG2 proteoglycan. Exp Neurol 2005, 192:299-309.
12. Fawcett J.W. Overcoming inhibition in the damaged spinal cord. J Neurotrauma 2006, 23:371-383.
13. Fawcett J.W., Asher R.A. The glial scar and central nervous system repair. Brain Res Bull 1999, 49:377-391.
14. Fenrich K.K., Rose P.K. Spinal interneuron axons spontaneously regenerate after spinal cord injury in the adult feline. J Neurosci 2009, 29:12145-12158.
15. Fenrich K.K., Rose P.K. Axons with highly branched terminal regions successfully regenerate across spinal midline transections in the adult cat. J Comp Neurol 2011, 519:3240-3258.
16. Fouad K., Klusman I., Schwab M.E. Regenerating corticospinal fibers in the Marmoset (Callitrix jacchus) after spinal cord lesion and treatment with the anti-Nogo-A antibody IN-1. Eur J Neurosci 2004, 20:2479-2482.
17. Freund P., Schmidlin E., Wannier T., Bloch J., Mir A., Schwab M.E., Rouiller E.M. Nogo-A-specific antibody treatment enhances sprouting and functional recovery after cervical lesion in adult primates. Nat Med 2006, 12:790-792.
18. Freund P., Schmidlin E., Wannier T., Bloch J., Mir A., Schwab M.E., Rouiller E.M. Anti-Nogo-A antibody treatment promotes recovery of manual dexterity after unilateral cervical lesion in adult primates - re-examination and extension of behavioral data. Eur J Neurosci 2009, 29:983-996.
19. Freund P., Wannier T., Schmidlin E., Bloch J., Mir A., Schwab M.E., Rouiller E.M. Anti-Nogo-A antibody treatment enhances sprouting of corticospinal axons rostral to a unilateral cervical spinal cord lesion in adult macaque monkey. J Comp Neurol 2007, 502:644-659.
20. Havton L., Kellerth J.O. Regeneration by supernumerary axons with synaptic terminals in spinal motoneurons of cats. Nature 1987, 325:711-714.
21. Inman D.M., Steward O. Ascending sensory, but not other long-tract axons, regenerate into the connective tissue matrix that forms at the site of a spinal cord injury in mice. J Comp Neurol 2003, 462:431-449.
22. Nordhausen K, Mottonen J, Oja H (2009) MNM: Multivariate Nonparametric Methods. An approach based on spatial signs and ranks. R package version 0.95-1.
23. Lee V.M., Otvos L., Carden M.J., Hollosi M., Dietzschold B., Lazzarini R.A. Identification of the major multiphosphorylation site in mammalian neurofilaments. Proc Natl Acad Sci U S A 1988, 85:1998-2002.
24. Liebscher T., Schnell L., Schnell D., Scholl J., Schneider R., Gullo M., Fouad K., Mir A., Rausch M., Kindler D., Hamers F.P.T., Schwab M.E. Nogo-A antibody improves regeneration and locomotion of spinal cord-injured rats. Ann Neurol 2005, 58:706-719.
25. Linda H., Cullheim S., Risling M. A light and electron microscopic study of intracellularly HRP-labeled lumbar motoneurons after intramedullary axotomy in the adult cat. J Comp Neurol 1992, 318:188-208.
26. Linda H., Risling M., Cullheim S. 'Dendraxons' in regenerating motoneurons in the cat: do dendrites generate new axons after central axotomy?. Brain Res 1985, 358:329-333.
27. 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.
28. Matthews M.A., St Onge M.F., Faciane C.L., Gelderd J.B. Axon sprouting into segments of rat spinal cord adjacent to the site of a previous transection. Neuropathol Appl Neurobiol 1979, 5:181-196.
29. McKeon R.J., Schreiber R.C., Rudge J.S., Silver J. Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J Neurosci 1991, 11:3398-3411.
30. Oertle T., Van der Haar M.E., Bandtlow C.E., Robeva A., Burfeind P., Buss A., Huber A.B., Simonen M., Schnell L., Brosamle C., Kaupmann K., Vallon R., Schwab M.E. Nogo-A inhibits neurite outgrowth and cell spreading with three discrete regions. J Neurosci 2003, 23:5393-5406.
31. Oja H., Randles R.H. Multivariate nonparametric tests. Stat Sci 2004, 19:598-605.
32. Pasterkamp R.J., Verhaagen J. Emerging roles for semaphorins in neural regeneration. Brain Res Brain Res Rev 2001, 35:36-54.
33. R Development Core Team (2008) A language and environment for statistical computing, Vienna, Austria.
34. Ramon y Cajal S. Degeneration and regeneration of the nervous system (May RM, translator) 1928, Oxford UP, New York.
35. Reier P.J., Stensaas L.J., Guth L. The astrocytic scar as an impediment to regeneration in the central nervous system. In the spinal cord reconstruction 1983, 163-195. Raven Press, New York.
36. Rudge J.S., Silver J. Inhibition of neurite outgrowth on astroglial scars in vitro. J Neurosci 1990, 10:3594-3603.
37. Schmidlin E., Wannier T., Bloch J., Belhaj-Saïf A., Wyss A., Rouiller E.M. Reduction of the hand representation in the ipsilateral primary motor cortex following unilateral section of the corticospinal tract at cervical level in monkeys. BMC Neurosci 2005, 6:56.
38. Schmidlin E., Wannier T., Bloch J., Rouiller E.M. Progressive plastic changes in the hand representation of the primary motor cortex parallel incomplete recovery from a unilateral section of the corticospinal tract at cervical level in monkeys. Brain Res 2004, 1017:172-183.
39. Schnell L., Schwab M.E. Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 1990, 343:269-272.
40. Schwab M.E. Repairing the injured spinal cord. Science 2002, 295:1029-1031.
41. Schwab M.E. Nogo and axon regeneration. Curr Opin Neurobiol 2004, 14:118-124.
42. Schwab M.E. Functions of Nogo proteins and their receptors in the nervous system. Nat Rev Neurosci 2010, 11:799-811.
43. Schwab M.E., Bartholdi D. Degeneration and regeneration of axons in the lesioned spinal cord. Physiol Rev 1996, 76:319-370.
44. Shearer M.C., Fawcett J.W. The astrocyte/meningeal cell interface - a barrier to successful nerve regeneration?. Cell Tissue Res 2001, 305:267-273.
45. Silver J., Miller J.H. Regeneration beyond the glial scar. Nat Rev Neurosci 2004, 5:146-156.
46. Sternberger L.A., Sternberger N.H. Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ. Proc Natl Acad Sci U S A 1983, 80:6126-6130.
47. Stichel C.C., Muller H.W. The CNS lesion scar: new vistas on an old regeneration barrier. Cell Tissue Res 1998, 294:1-9.
48. Thallmair M., Metz G.A.S., Z'Graggen W.J., Raineteau O., Kartje G.L., Schwab M.E. Neurite growth inhibitors restrict plasticity and functional recovery following corticospinal tract lesions. Nat Neurosci 1998, 1:124-131.
49. Tsang Y.M., Chiong F., Kuznetsov D., Kasarskis E., Geula C. Motor neurons are rich in non-phosphorylated neurofilaments: cross-species comparison and alterations in ALS. Brain Res 2000, 861:45-58.
50. Wallace M.C., Tator C.H., Lewis A.J. Chronic regenerative changes in the spinal cord after cord compression injury in rats. Surg Neurol 1987, 27:209-219.
51. Wang Z.H., Walter G.F., Gerhard L. The expression of nerve growth factor receptor on Schwann cells and the effect of these cells on the regeneration of axons in traumatically injured human spinal cord. Acta Neuropathol 1996, 91:180-184.
52. Wannier T., Schmidlin E., Bloch J., Rouiller E.M. A unilateral section of the corticospinal tract at cervical level in primate does not lead to measurable cell loss in motor cortex. J Neurotrauma 2005, 22:703-717.
53. Wannier-Morino P., Schmidlin E., Freund P., Belhaj-Saif A., Bloch J., Mir A., Schwab M.E., Rouiller E.M., Wannier T. Fate of rubrospinal neurons after unilateral section of the cervical spinal cord in adult macaque monkeys: effects of an antibody treatment neutralizing Nogo-A. Brain Res 2008, 1217:96-109.
54. Weinmann O., Schnell L., Ghosh A., Montani L., Wiessner C., Wannier T., Rouiller E., Mir A., Schwab M.E. Intrathecally infused antibodies against Nogo-A penetrate the CNS and downregulate the endogenous neurite growth inhibitor Nogo-A. Mol Cell Neurosci 2006, 32:161-173.