Delayed anti-Nogo-A antibody application after spinal cord injury shows progressive loss of responsiveness

Journal of Neurotrauma

Volumn 29, Issue 3, 2012, Pages 567-578

  Gonzenbach, Roman R ^a   Zoerner, Bjoern ^b   Schnell, Lisa ^b   Weinmann, Oliver ^b   Mir, Anis K ^c   Schwab, Martin E ^d  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c NOVARTIS PHARMA AG   (Switzerland)

^d ETH ZURICH   (Switzerland)

Author keywords

delayed treatment; motor function; Nogo A; plasticity; recovery; spinal cord injury; sprouting

Indexed keywords

MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 11C7; NOGO A ANTIBODY; PROTEOCHONDROITIN SULFATE; PROTEOGLYCAN CS 56; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ARTICLE; CHRONOTHERAPY; CONTINUOUS INFUSION; CONTROLLED STUDY; DRUG CEREBROSPINAL FLUID LEVEL; DRUG RESPONSE; DRUG SCREENING; FEMALE; IMMUNOREACTIVITY; IMMUNOTHERAPY; MOTOR PERFORMANCE; NERVE FIBER REGENERATION; NONHUMAN; OPEN FIELD BEHAVIOR; PYRAMIDAL TRACT; RAT; SPINAL CORD INJURY; THERAPY DELAY;

ANIMALS; ANTIBODIES, BLOCKING; CHONDROITIN SULFATE PROTEOGLYCANS; DISEASE PROGRESSION; FEMALE; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MYELIN PROTEINS; NERVE REGENERATION; POSTURAL BALANCE; PYRAMIDAL TRACTS; RATS; RATS, INBRED LEW; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; SWIMMING;

EID: 84857263418     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2011.1752     Document Type: Article

References (52)

1. Avnur, Z., and Geiger, B. (1984). Immunocytochemical localization of native chondroitin-sulfate in tissues and cultured cells using specific monoclonal antibody. Cell 38, 811-822. (Pubitemid 15176111)
2. Bareyre, F.M., Haudenschild, B., and Schwab, M.E. (2002). Long-lasting sprouting and gene expression changes induced by the monoclonal antibody IN-1 in the adult spinal cord. J. Neu-rosci. 22, 7097-7110. (Pubitemid 35379165)
3. Basso, D.M., Beattie, M.S., and Bresnahan, J.C. (1995). A sensitive and reliable locomotor rating scale for open field testing in rats. J. Neurotrauma 12, 1-21.
4. Basso, D.M. (2004). Behavioral testing after spinal cord injury: congruities, complexities, and controversies. J. Neurotrauma 21, 395-404. (Pubitemid 38509423)
5. Busch, S.A., and Silver, J. (2007). The role of extracellular matrix in CNS regeneration. Curr. Opin. Neurobiol. 17, 120-127. (Pubitemid 46227979)
6. Cafferty, W.B., and Strittmatter, S.M. (2006). The Nogo-Nogo receptor pathway limits a spectrum of adult CNS axonal growth. J. Neurosci. 26, 12242-12250. (Pubitemid 44808391)
7. Cafferty, W.B., Duffy, P., Huebner, E., and Strittmatter, S.M. (2010). MAG and OMgp synergize with Nogo-A to restrict axonal growth and neurological recovery after spinal cord trauma. J. Neurosci. 30, 6825-6837.
8. Cafferty, W.B., Kim, J.E., Lee, J.K., and Strittmatter, S.M. (2007). Response to correspondence: Kim et al., "axon regeneration in young adult mice lacking Nogo-A/B." Neuron 38, 187-199. Neuron 54, 195-199. (Pubitemid 46561211)
9. Camand, E., Morel, M.P., Faissner, A., Sotelo, C., and Dusart, I. (2004). Long-term changes in the molecular composition of the glial scar and progressive increase of serotoninergic fibre sprouting after hemisection of the mouse spinal cord. Eur. J. Neurosci. 20, 1161-1176. (Pubitemid 39233570)
10. Canty, A.J., and Murphy, M. (2008). Molecular mechanisms of axon guidance in the developing corticospinal tract. Prog. Neurobiol. 85, 214-235.
11. Dimou, L., Schnell, L., Montani, L., Duncan, C., Simonen, M., Schneider, R., Liebscher, T., Gullo, M., and Schwab, M.E. (2006). Nogo-A-deficient mice reveal strain-dependent differences in axonal regeneration. J. Neurosci. 26, 5591-5603. (Pubitemid 44315252)
12. Ditunno, J.F., Little, J.W., Tessler, A., and Burns, A.S. (2004). Spinal shock revisited: a four-phase model. Spinal Cord 42, 383-395. (Pubitemid 38969649)
13. Dodd, D.A., Niederoest, B., Bloechlinger, S., Dupuis, L., Loeffler, J.P., and Schwab, M.E. (2005). Nogo-A,-B, and-C are found on the cell surface and interact together in many different cell types. J. Biol. Chem. 280, 12494-12502.
14. Freund, P., Schmidlin, E., Wannier, T., Bloch, J., Mir, A., Schwab, M.E., and Rouiller, E.M. (2006). Nogo-A-specific antibody treatment enhances sprouting and functional recovery after cervical lesion in adult primates. Nat. Med. 12, 790-792. (Pubitemid 44050068)
15. Gonzenbach, R.R., and Schwab, M.E. (2008). Disinhibition of neurite growth to repair the injured adult CNS: focusing on Nogo. Cell Mol. Life Sci. 65, 161-176.
16. Gonzenbach, R.R., Gasser, P., Zorner, B., Hochreutener, E., Dietz, V., and Schwab, M.E. (2010). Nogo-A antibodies and training reduce muscle spasms in spinal cord-injured rats. Ann. Neurol. 68, 48-57.
17. Herzog, A., and Brosamle, C. (1997). 'Semifree-floating' treatment: a simple and fast method to process consecutive sections for immunohistochemistry and neuronal tracing. J. Neurosci. Methods 72, 57-63. (Pubitemid 27154188)
18. Hiersemenzel, L.P., Curt, A., and Dietz, V. (2000). From spinal shock to spasticity: neuronal adaptations to a spinal cord injury. Neurology 54, 1574-1582. (Pubitemid 30226799)
19. Houle, J.D. (1991). Demonstration of the potential for chronically injured neurons to regenerate axons into intraspinal peripheral nerve grafts. Exp. Neurol. 113, 1-9.
20. Hua, J.Y., and Smith, S.J. (2004). Neural activity and the dynamics of central nervous system development. Nat. Neurosci. 7, 327-332. (Pubitemid 38429168)
21. Jones, L.L., Yamaguchi, Y., Stallcup, W.B., and Tuszynski, M.H. (2002). NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macro-phages and oligodendrocyte progenitors. J. Neurosci. 22, 2792-2803. (Pubitemid 37465828)
22. Juvin, L., Simmers, J., and Morin, D. (2005). Propriospinal circuitry underlying interlimb coordination in mammalian quadrupedal locomotion. J. Neurosci. 25, 6025-6035. (Pubitemid 40911434)
23. Kim, J.E., Li, S., GrandPre, T., Qiu, D., and Strittmatter, S.M. (2003). Axon regeneration in young adult mice lacking Nogo-A/B. Neuron 38, 187-199. (Pubitemid 36555646)
24. Kwon, B.K., Liu, J., Messerer, C., Kobayashi, N.R., McGraw, J., Oschipok, L., and Tetzlaff, W. (2002). Survival and regeneration of rubrospinal neurons 1 year after spinal cord injury. Proc. Natl. Acad. Sci. USA 99, 3246-3251. (Pubitemid 34240617)
25. Lee, J.K., Chan, A.F., Luu, S.M., Zhu, Y., Ho, C., Tessier-Lavigne, M., and Zheng, B. (2009). Reassessment of corticospinal tract regeneration in Nogo-deficient mice. J. Neurosci. 29, 8649-8654.
26. Lee, J.K., Geoffroy, C.G., Chan, A.F., Tolentino, K.E., Crawford, M.J., Leal, M.A., Kang, B., and Zheng, B. (2010). Assessing spinal axon regeneration and sprouting in Nogo-, MAG-, and OMgp-deficient mice. Neuron 66, 663-670.
27. Li, S., and Strittmatter, S.M. (2003). Delayed systemic Nogo-66 receptor antagonist promotes recovery from spinal cord injury. J. Neurosci. 23, 4219-4227. (Pubitemid 36958442)
28. Liebscher, T., Schnell, L., Schnell, D., Scholl, J., Schneider, R., Gullo, M., Fouad, K., Mir, A., Rausch, M., Kindler, D., Ha-mers, F.P., and Schwab, M.E. (2005). Nogo-A antibody improves regeneration and locomotion of spinal cord-injured rats. Ann. Neurol. 58, 706-719. (Pubitemid 41552546)
29. Markus, T.M., Tsai, S.Y., Bollnow, M.R., Farrer, R.G., O'Brien, T.E., Kindler-Baumann, D.R., Rausch, M., Rudin, M., Wiess-ner, C., Mir, A.K., Schwab, M.E., and Kartje, G.L. (2005). Recovery and brain reorganization after stroke in adult and aged rats. Ann. Neurol. 58, 950-953. (Pubitemid 41746886)
30. Martin, J.H. (2005). The corticospinal system: from development to motor control. Neuroscientist 11, 161-173. (Pubitemid 40388498)
31. McKeon, R.J., Jurynec, M.J., and Buck, C.R. (1999). The chon-droitin sulfate proteoglycans neurocan and phosphacan are expressed by reactive astrocytes in the chronic CNS glial scar. J. Neurosci. 19, 10778-10788. (Pubitemid 30235724)
32. 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., and Schwab, M.E. (2003). Nogo-A inhibits neurite outgrowth and cell spreading with three discrete regions. J. Neurosci. 23, 5393-5406. (Pubitemid 36807813)
33. Pallini, R., Fernandez, E., and Sbriccoli, A. (1988). Retrograde degeneration of corticospinal axons following transection of the spinal cord in rats. A quantitative study with ante-rogradely transported horseradish peroxidase. J. Neurosurg. 68, 124-128. (Pubitemid 18019142)
34. Plunet, W., Kwon, B.K., and Tetzlaff, W. (2002). Promoting ax-onal regeneration in the central nervous system by enhancing the cell body response to axotomy. J. Neurosci. Res. 68, 1-6. (Pubitemid 34274991)
35. Schnell, L., and Schwab, M.E. (1990). Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 343, 268-272.
36. Schwab, M.E. (2010). Mutant mice challenged as models of injury in the central nervous system. Nature Med. 16, 860.
37. Schwab, M.E. (2004). Nogo and axon regeneration. Curr. Opin. Neurobiol. 14, 118-124. (Pubitemid 38264581)
38. Seif, G.I., Nomura, H., and Tator, C.H. (2007). Retrograde axonal degeneration "dieback" in the corticospinal tract after tran-section injury of the rat spinal cord: a confocal microscopy study. J. Neurotrauma 24, 1513-1528. (Pubitemid 47493515)
39. Seymour, A.B., Andrews, E.M., Tsai, S.Y., Markus, T.M., Boll-now, M.R., Brenneman, M.M., O'Brien, T.E., Castro, A.J., Schwab, M.E., and Kartje, G.L. (2005). Delayed treatment with monoclonal antibody IN-1 1 week after stroke results in recovery of function and corticorubral plasticity in adult rats. J. Cereb. Blood Flow Metab. 25, 1366-1375. (Pubitemid 41348738)
40. Simonen, M., Pedersen, V., Weinmann, O., Schnell, L., Buss, A., Ledermann, B., Christ, F., Sansig, G., van der Putten, H., and Schwab, M.E. (2003). Systemic deletion of the myelin-asso-ciated outgrowth inhibitor Nogo-A improves regenerative and plastic responses after spinal cord injury. Neuron 38, 201-211. (Pubitemid 36555647)
41. Steward, O., Zheng, B., Banos, K., and Yee, K.M. (2007). Response to: Kim et al., "axon regeneration in young adult mice lacking Nogo-A/B." Neuron 38, 187-199. Neuron 54, 191-195. (Pubitemid 46561210)
42. Tang, X., Davies, J.E., and Davies, S.J. (2003). Changes in distribution, cell associations, and protein expression levels of NG2, neurocan, phosphacan, brevican, versican V2, and te-nascin-C during acute to chronic maturation of spinal cord scar tissue. J. Neurosci. Res. 71, 427-444. (Pubitemid 36159501)
43. Tsai, S.Y., Markus, T.M., Andrews, E.M., Cheatwood, J.L., Emerick, A.J., Mir, A.K., Schwab, M.E., and Kartje, G.L. (2007). Intrathecal treatment with anti-Nogo-A antibody improves functional recovery in adult rats after stroke. Exp. Brain Res. 182, 261-266. (Pubitemid 350218894)
44. Tsai, S.Y., Papadopoulos, C., Schwab, M.E., and Kartje, G.L. (2010). Delayed anti-Nogo-A therapy enhances functional improvement and axonal plasticity after chronic stroke in adult rats. Stroke 42, 186-190.
45. Tuszynski, M.H. (2010). Mutant mice challenged as models of injury in the central nervous system. Nature Med. 16, 860.
46. von Meyenburg, J., Brosamle, C., Metz, G.A., and Schwab, M.E. (1998). Regeneration and sprouting of chronically injured corticospinal tract fibers in adult rats promoted by NT-3 and the mAb IN-1, which neutralizes myelin-associated neurite growth inhibitors. Exp. Neurol. 154, 583-594.
47. Wannier, T., Schmidlin, E., Bloch, J., and Rouiller, E.M. (2005). A unilateral section of the corticospinal tract at cervical level in primate does not lead to measurable cell loss in motor cortex. J. Neurotrauma 22, 703-717. (Pubitemid 40840384)
48. Weinmann, O., Schnell, L., Ghosh, A., Montani, L., Wiessner, C., Wannier, T., Rouiller, E., Mir, A., and Schwab, M.E. (2006). Intrathecally infused antibodies against Nogo-A penetrate the CNS and downregulate the endogenous neurite growth inhibitor Nogo-A. Mol. Cell Neurosci. 32, 161-173. (Pubitemid 43868104)
49. Ye, J.H., and Houle, J.D. (1997). Treatment of the chronically injured spinal cord with neurotrophic factors can promote axonal regeneration from supraspinal neurons. Exp. Neurol. 143, 70-81. (Pubitemid 27049133)
50. Yiu, G., and He, Z. (2006). Glial inhibition of CNS axon regeneration. Nat. Rev. Neurosci. 7, 617-627. (Pubitemid 44106744)
51. Ylera, B., Erturk, A., Hellal, F., Nadrigny, F., Hurtado, A., Ta-hirovic, S., Oudega, M., Kirchhoff, F., and Bradke, F. (2009). Chronically CNS-injured adult sensory neurons gain regen-erative competence upon a lesion of their peripheral axon. Curr. Biol. 19, 930-936.
52. Zheng, B., Ho, C., Li, S., Keirstead, H., Steward, O., and Tessier-Lavigne, M. (2003). Lack of enhanced spinal regeneration in Nogo-deficient mice. Neuron 38, 213-224. (Pubitemid 36555648)