Delayed systemic Nogo-66 receptor antagonist promotes recovery from spinal cord injury

Journal of Neuroscience

Volumn 23, Issue 10, 2003, Pages 4219-4227

  Li, Shuxin ^a   Strittmatter, Stephen M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Axon regeneration; NEP1 40 peptide; Nogo; Nogo 66 receptor antagonist; Serotonergic fiber; Spinal cord injury; SPRR1A; Trauma

Indexed keywords

CELL PROTEIN; MYELIN ASSOCIATED GLYCOPROTEIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; NOGO 66 RECEPTOR; NOGO66 RECEPTOR ANTAGONIST; PROLINE DERIVATIVE; PROTEIN NEP[1-40]; PROTEIN NOGO; PROTEIN SPRR1A; RECEPTOR PROTEIN; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; CORNIFINS; MEMBRANE PROTEIN; MYELIN PROTEIN; NEPI 40 PROTEIN, MOUSE; NEPI-40 PROTEIN, MOUSE; PEPTIDE FRAGMENT; PROTEIN; RTN4R PROTEIN, MOUSE; RTN4R PROTEIN, RAT; SEROTONIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; COMPETITIVE INHIBITION; CONTROLLED STUDY; CONVALESCENCE; DOSE TIME EFFECT RELATION; DRUG MECHANISM; DRUG POTENCY; FEMALE; LOCOMOTION; MAMMAL; MOUSE; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PYRAMIDAL TRACT; RECEPTOR BINDING; SEROTONIN RELEASE; SPINAL CORD INJURY; SPINAL CORD TRANSSECTION; SURGICAL APPROACH; THORACIC SPINE; AMINO ACID SEQUENCE; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; INJURY; METABOLISM; MOLECULAR GENETICS; MOLECULAR WEIGHT; MOTOR ACTIVITY; NERVE FIBER; NERVE FIBER TRANSECTION; NERVE REGENERATION; PHYSIOLOGY; PROTEIN SYNTHESIS; SPINAL CORD; SPINAL GANGLION; SUBCUTANEOUS DRUG ADMINISTRATION; THALAMUS INTRALAMINAR NUCLEUS;

AMINO ACID SEQUENCE; ANIMALS; AXONS; AXOTOMY; BEHAVIOR, ANIMAL; FEMALE; GANGLIA, SPINAL; INJECTIONS, SUBCUTANEOUS; INTRALAMINAR THALAMIC NUCLEI; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; MOTOR ACTIVITY; MYELIN PROTEINS; NERVE FIBERS; NERVE REGENERATION; PEPTIDE FRAGMENTS; PROTEIN BIOSYNTHESIS; PROTEINS; PYRAMIDAL TRACTS; RECEPTORS, CELL SURFACE; SEROTONIN; SPINAL CORD; SPINAL CORD INJURIES;

EID: 0038042274     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-10-04219.2003     Document Type: Article

References (50)

1. Bartsch U, Bandtlow CE, Schnell L, Bartsch S, Spillmann AA, Rubin BP, Hillenbrand R, Montag D, Schwab ME, Schachner M (1995) Lack of evidence that myelin-associated glycoprotein is a major inhibitor of axonal regeneration in the CNS. Neuron 15:1375-1381.
2. Basso DM, Beattie MS, Bresnahan JC, Anderson DK, Faden AI, Gruner JA, Holford TR, Hsu CY, Noble LJ, Nockels R, Perot PL, Salzman SK, Young W (1996) MASCIS evaluation of open field locomotor scores: effects of experience and teamwork on reliability. Multicenter Animal Spinal Cord Injury Study. J Neurotrauma 13:343-359.
3. Bomze HM, Bulsara KR, Iskandar BJ, Caroni P, Skene JH (2001) Spinal axon regeneration evoked by replacing two growth cone proteins in adult neurons. Nat Neurosci 4:38-43.
4. Bonilla IE, Tanabe K, Strittmatter SM (2002) Small proline-rich repeat protein 1A is expressed by axotomized neurons and promotes axonal outgrowth. J Neurosci 22:1303-1315.
5. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416:636-640.
6. Bregman BS, Kunkel-Bagden E, Reier PJ, Dai HN, McAtee M, Gao D (1993) Recovery of function after spinal cord injury: mechanisms underlying transplant-mediated recovery of function differ after spinal cord injury in newborn and adult rats. Exp Neurol 123:3-16.
7. Bregman BS, Kunkel-Bagden E, Schnell L, Dai HN, Gao D, Schwab ME (1995) Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature 378:498-501.
8. Brosamle C, Schwab ME (1997) Cells of origin, course, and termination patterns of the ventral, uncrossed component of the mature rat corticospinal tract. J Comp Neurol 386:293-303.
9. Brosamle C, Huber AB, Fiedler M, Skerra A, Schwab ME (2000) Regeneration of lesioned corticospinal tract fibers in the adult rat induced by a recombinant, humanized IN-1 antibody fragment. J Neurosci 20:8061-8068.
10. Brustein E, Rossignol S (1998) Recovery of locomotion after ventral and ventrolateral spinal lesions in the cat: I. Deficits and adaptive mechanisms. J Neurophysiol 80:1245-1267.
11. Cavaletti G, Oggioni N, Sala F, Pezzoni G, Cavalletti E, Marmiroli P, Petruccioli MG, Frattola L, Tredici G (2000) Effect on the peripheral nervous system of systemically administered dimethylsulfoxide in the rat: a neurophysiological and pathological study. Toxicol Lett 118:103-107.
12. Chen MS, Huber AB, van der Haar ME, Frank M, Schnell L, Spillmann AA, Christ F, Schwab ME (2000) Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 403:434-439.
13. Coumans W, Lin TT, Dai HN, MacArthur L, McAtee M, Nash C, Bregman BS (2001) Axonal regeneration and functional recovery after complete spinal cord transection in rats by delayed treatment with transplants and neurotrophins. J Neurosci 21:9334-9344.
14. Davies SJ, Goucher DR, Doller C, Silver J (1999) Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J Neurosci 19:5810-5822.
15. Dergham P, Ellezam B, Essagian C, Avedissian H, Lubell WD, McKerracher L (2002) Rho signaling pathway targeted to promote spinal cord repair. J Neurosci 22:6570-6577.
16. Domeniconi M, Cao Z, Spencer T, Sivasankaran R, Wang K, Nikulina E, Kimura N, Cai H, Deng K, Gao Y, He Z, Filbin M (2002) Myelin-associated glycoprotein interacts with the nogo66 receptor to inhibit neurite outgrowth. Neuron 35:283.
17. Dou CL, Levine JM (1994) Inhibition of neurite growth by the NG2 chondroitin sulfate proteoglycan. J Neurosci 14:7616-7628.
18. Fournier AE, GrandPre T, Strittmatter SM (2001) Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 409:341-346.
19. Goldberg JL, Klassen MP, Hua Y, Barres BA (2002) Amacrine-signaled loss of intrinsic axon growth ability by retinal ganglion cells. Science 296:1860-1864.
20. GrandPre T, Nakamura F, Vartanian T, Strittmatter SM (2000) Identification of the Nogo inhibitor of axon regeneration as a Reticulon protein. Nature 403:439-444.
21. GrandPre T, Li S, Strittmatter SM (2002) Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature 417:547-551.
22. Huang DW, McKerracher L, Braun PE, David S (1999) A therapeutic vaccine approach to stimulate axon regeneration in the adult mammalian spinal cord. Neuron 24:639-647.
23. Li Y, Field PM, Raisman G (1997) Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 277:2000-2002.
24. Liu BP, Fournier A, GrandPre T, Strittmatter SM (2002) Myelin-associated glycoprotein as a functional ligand for the nogo-66 receptor. Science 297:1190-1193.
25. Liu RY, Snider WD (2001) Different signaling pathways mediate regenerative versus developmental sensory axon growth. J Neurosci 21:RC164.
26. McKerracher L, David S, Jackson DL, Kottis V, Dunn RJ, Braun PE (1994) Identification of myelin-associated glycoprotein as a major myelin-derived inhibitor of neurite growth. Neuron 13:805-811.
27. Metz GA, Merkler D, Dietz V, Schwab ME, Fouad K (2000) Efficient testing of motor function in spinal cord injured rats. Brain Res 883:165-177.
28. Mukhopadhyay G, Doherty P, Walsh FS, Crocker PR, Filbin MT (1994) A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron 13:757-767.
29. Neumann S, Bradke F, Tessier-Lavigne M, Basbaum AI (2002) Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 34:885-893.
30. Prinjha R, Moore SE, Vinson M, Blake S, Morrow R, Christie G, Michalovich D, Simmons DL, Walsh FS (2000) Inhibitor of neurite outgrowth in humans. Nature 403:383-384.
31. Qiu J, Cai D, Dai H, McAtee M, Hoffman PN, Bregman BS, Filbin MT (2002) Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34:895-903.
32. Raineteau O, Fouad K, Noth P, Thallmair M, Schwab ME (2001) Functional switch between motor tracts in the presence of the mAb IN-1 in the adult rat. Proc Natl Acad Sci USA 98:6929-6934.
33. Ramon-Cueto A, Cordero MI, Santos-Benito FF, Avila J (2000) Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 25:425-435.
34. Richardson PM, McGuinness UM, Aguayo AJ (I980) Axons from CNS neurons regenerate into PNS grafts. Nature 284:264-265.
35. Savio T, Schwab ME (1990) Lesioned corticospinal tract axons regenerate in myelin-free rat spinal cord. Proc Natl Acad Sci USA 87:4130-4133.
36. Schafer M, Fruttiger M, Montag D, Schachner M, Martini R (1996) Disruption of the gene for the myelin-associated glycoprotein improves axonal regrowth along myelin in C57BL/Wlds mice. Neuron 16:1107-1113.
37. Schnell L, Schneider R, Kolbeck R, Barde YA, Schwab ME (1994) Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 367:170-173.
38. Schnell L, Fearn S, Klassen H, Schwab ME, Perry VH (1999) Acute inflammatory responses to mechanical lesions in the CNS: differences between brain and spinal cord. Eur J Neurosci 11:3648-3658.
39. Schucht P, Raineteau O, Schwab ME, Fouad K (2002) Anatomical correlates of locomotor recovery following dorsal and ventral lesions of the rat spinal cord. Exp Neurol 176:143-153.
40. Snow DM, Lemmon V, Carrino DA, Caplan AI, Silver J (1990) Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp Neurol 109:111-130.
41. Steward O, Schauwecker PE, Guth L, Zhang Z, Fujiki M, Inman D, Wrathall J, Kempermann G, Gage FH, Saatman KE, Raghupathi R, McIntosh T (1999) Genetic approaches to neurotrauma research: opportunities and potential pitfalls of murine models. Exp Neurol 157:19-42.
42. Takami T, Oudega M, Bates ML, Wood PM, Kleitman N, Bunge MB (2002) Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J Neurosci 22:6670-6681.
43. Thallmair M, Metz GA, Z'Graggen WJ, Raineteau O, Kartje GL, Schwab ME (1998) Neurite growth inhibitors restrict plasticity and functional recovery following corticospinal tract lesions. Nat Neurosci 1:124-131.
44. von Meyenburg J, Brosamle C, Metz GA, Schwab ME (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.
45. Wang KC, Koprivica V, Kim JA, Sivasankaran R, Guo Y, Neve RL, He Z (2002a) Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 417:941-944.
46. Wang KC, Kim JA, Sivasankaran R, Segal R, He Z (2002b) P75 interacts with the Nogo receptor as a co-receptor for Nogo, MAG and OMgp. Nature 420:74-78.
47. Wang X, Chun SJ, Treloar H, Vartanian T, Greer CA, Strittmatter SM (2002) Localization of Nogo-A and Nogo-66 receptor proteins at sites of axon-myelin and synaptic contact. J Neurosci 22:5505-5515.
48. Weidner N, Ner A, Salimi N, Tuszynski MH (2001) Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. Proc Natl Acad Sci USA 98:3513-3518.
49. Wong ST, Henley JR, Kanning KC, Huang KH, Bothwell M, Poo MM (2002) A p75(NTR) and Nogo receptor complex mediates repulsive signaling by myelin-associated glycoprotein. Nat Neurosci 5:1302-1308.
50. Ye JH, Houle JD (1997) Treatment of the chronically injured spinal cord with neurotrophic factors can promote axonal regeneration from supraspinal neurons. Exp Neurol 143:70-81.