Axonal regeneration induced by blockade of glial inhibitors coupled with activation of intrinsic neuronal growth pathways

Experimental Neurology

Volumn 237, Issue 1, 2012, Pages 55-69

  Wang, Xingxing ^a   Hasan, Omar ^a   Arzeno, Alexander ^a   Benowitz, Larry I ^b   Cafferty, William B J ^a   Strittmatter, Stephen M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Axon regeneration; Chondroitin sulfate proteoglycan; Myelin; Nogo; Nogo receptor; Optic nerve regeneration; Preconditioning; Spinal cord injury

Indexed keywords

CHONDROITIN 4 SULFATE; CHONDROITIN ABC LYASE; IMMUNOGLOBULIN G; ISOFLURANE; MEMBRANE RECEPTOR; NOGO RECEPTOR; NOGO RECEPTOR 1; PARAFORMALDEHYDE; UNCLASSIFIED DRUG; ZYMOSAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; CONTROLLED STUDY; CRYOPROTECTION; ENZYME ACTIVATION; FEMALE; GENE DELETION; GLIA; IMMUNOREACTIVITY; LAMINECTOMY; MOUSE; NERVE FIBER REGENERATION; NERVE FIBER TRANSECTION; NONHUMAN; OPTIC NERVE; OPTIC NERVE INJURY; OSMOTIC PUMP; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; RETINA GANGLION CELL; SCIATIC NERVE; SPINAL CORD DORSAL HORN; SPINAL CORD INJURY;

ANIMALS; AXONS; CHONDROITIN ABC LYASE; FEMALE; GPI-LINKED PROTEINS; MACROPHAGE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELIN PROTEINS; NEURAL INHIBITION; NEUROGLIA; OPTIC NERVE INJURIES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CELL SURFACE; SPINAL CORD INJURIES; ZYMOSAN;

EID: 84863812381     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.06.009     Document Type: Article

References (79)

1. Alilain W.J., Li X., Horn K.P., Dhingra R., Dick T.E., Herlitze S., Silver J. Light-induced rescue of breathing after spinal cord injury. J. Neurosci. 2008, 28:11862-11870.
2. Alto L.T., Havton L.A., Conner J.M., Hollis Ii E.R., Blesch A., Tuszynski M.H. Chemotropic guidance facilitates axonal regeneration and synapse formation after spinal cord injury. Nat. Neurosci. 2009, 12:1106-1113.
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. Barton W.A., Liu B.P., Tzvetkova D., Jeffrey P.D., Fournier A.E., Sah D., Cate R., Strittmatter S.M., Nikolov D.B. Structure and axon outgrowth inhibitor binding of the Nogo-66 receptor and related proteins. EMBO J. 2003, 22:3291-3302.
5. Benfey M., Aguayo A.J. Extensive elongation of axons from rat brain into peripheral nerve grafts. Nature 1982, 296:150-152.
6. Benowitz L.I., Goldberg D.E., Madsen J.R., Soni D., Irwin N. Inosine stimulates extensive axon collateral growth in the rat corticospinal tract after injury. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:13486-13490.
7. Benson M.D., Romero M.I., Lush M.E., Lu Q.R., Henkemeyer M., Parada L.F. Ephrin-B3 is a myelin-based inhibitor of neurite outgrowth. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:10694-10699.
8. Blesch A., Lu P., Tsukada S., Alto L.T., Roet K., Coppola G., Geschwind D., Tuszynski M.H. Conditioning lesions before or after spinal cord injury recruit broad genetic mechanisms that sustain axonal regeneration: superiority to camp-mediated effects. Exp. Neurol. 2011, 235:162-173.
9. Bradbury E.J., Khemani S., King Von R., Priestley J.V., McMahon S.B. NT-3 promotes growth of lesioned adult rat sensory axons ascending in the dorsal columns of the spinal cord. Eur. J. Neurosci. 1999, 11:3873-3883.
10. Bradbury E.J., Moon L.D., Popat R.J., King V.R., Bennett G.S., Patel P.N., Fawcett J.W., McMahon S.B. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002, 416:636-640.
11. Bregman B.S., McAtee M., Dai H.N., Kuhn P.L. Neurotrophic factors increase axonal growth after spinal cord injury and transplantation in the adult rat. Exp. Neurol. 1997, 148:475-494.
12. Cafferty W.B., Strittmatter S.M. The Nogo-Nogo receptor pathway limits a spectrum of adult CNS axonal growth. J. Neurosci. 2006, 26:12242-12250.
13. Cafferty W.B., Yang S.H., Duffy P.J., Li S., Strittmatter S.M. Functional axonal regeneration through astrocytic scar genetically modified to digest chondroitin sulfate proteoglycans. J. Neurosci. 2007, 27:2176-2185.
14. Cafferty W.B., Bradbury E.J., Lidierth M., Jones M., Duffy P.J., Pezet S., McMahon S.B. Chondroitinase ABC-mediated plasticity of spinal sensory function. J. Neurosci. 2008, 28:11998-12009.
15. Caggiano A.O., Zimber M.P., Ganguly A., Blight A.R., Gruskin E.A. Chondroitinase ABCI improves locomotion and bladder function following contusion injury of the rat spinal cord. J. Neurotrauma 2005, 22:226-239.
16. Carter L.M., Starkey M.L., Akrimi S.F., Davies M., McMahon S.B., Bradbury E.J. The yellow fluorescent protein (YFP-H) mouse reveals neuroprotection as a novel mechanism underlying chondroitinase ABC-mediated repair after spinal cord injury. J. Neurosci. 2008, 28:14107-14120.
17. 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.
18. Chen P., Goldberg D.E., Kolb B., Lanser M., Benowitz L.I. Inosine induces axonal rewiring and improves behavioral outcome after stroke. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:9031-9036.
19. Courtine G., Song B., Roy R.R., Zhong H., Herrmann J.E., Ao Y., Qi J., Edgerton V.R., Sofroniew M.V. Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat. Med. 2008, 14:69-74.
20. David S., Aguayo A.J. Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science 1981, 214:931-933.
21. Fang P.C., Barbay S., Plautz E.J., Hoover E., Strittmatter S.M., Nudo R.J. Combination of NEP 1-40 treatment and motor training enhances behavioral recovery after a focal cortical infarct in rats. Stroke 2010, 41:544-549.
22. 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.
23. Fournier A.E., GrandPre T., Strittmatter S.M. Identification of a receptor mediating Nogo-66 inhibition of axonal regeneration. Nature 2001, 409:341-346.
24. 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.
25. Garcia-Alias G., Barkhuysen S., Buckle M., Fawcett J.W. Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation. Nat. Neurosci. 2009, 12:1145-1151.
26. 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.
27. Hagg T., Baker K.A., Emsley J.G., Tetzlaff W. Prolonged local neurotrophin-3 infusion reduces ipsilateral collateral sprouting of spared corticospinal axons in adult rats. Neuroscience 2005, 130:875-887.
28. Harel N.Y., Song K.H., Tang X., Strittmatter S.M. Nogo receptor deletion and multimodal exercise improve distinct aspects of recovery in cervical spinal cord injury. J. Neurotrauma 2010, 27:2055-2066.
29. Harvey P.A., Lee D.H., Qian F., Weinreb P.H., Frank E. Blockade of Nogo receptor ligands promotes functional regeneration of sensory axons after dorsal root crush. J. Neurosci. 2009, 29:6285-6295.
30. Hata K., Fujitani M., Yasuda Y., Doya H., Saito T., Yamagishi S., Mueller B.K., Yamashita T. RGMa inhibition promotes axonal growth and recovery after spinal cord injury. J. Cell Biol. 2006, 173:47-58.
31. Ikegami T., Nakamura M., Yamane J., Katoh H., Okada S., Iwanami A., Watanabe K., Ishii K., Kato F., Fujita H., Takahashi T., Okano H.J., Toyama Y., Okano H. Chondroitinase ABC combined with neural stem/progenitor cell transplantation enhances graft cell migration and outgrowth of growth-associated protein-43-positive fibers after rat spinal cord injury. Eur. J. Neurosci. 2005, 22:3036-3046.
32. Ji B., Li M., Budel S., Pepinsky R.B., Walus L., Engber T.M., Strittmatter S.M., Relton J.K. Effect of combined treatment with methylprednisolone and soluble Nogo-66 receptor after rat spinal cord injury. Eur. J. Neurosci. 2005, 22:587-594.
33. Kadoya K., Tsukada S., Lu P., Coppola G., Geschwind D., Filbin M.T., Blesch A., Tuszynski M.H. Combined intrinsic and extrinsic neuronal mechanisms facilitate bridging axonal regeneration one year after spinal cord injury. Neuron 2009, 64:165-172.
34. 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.
35. Kim J.E., Liu B.P., Park J.H., Strittmatter S.M. Nogo-66 receptor prevents raphespinal and rubrospinal axon regeneration and limits functional recovery from spinal cord injury. Neuron 2004, 44:439-451.
36. Kurimoto T., Yin Y., Omura K., Gilbert H.Y., Kim D., Cen L.P., Moko L., Kugler S., Benowitz L.I. Long-distance axon regeneration in the mature optic nerve: contributions of oncomodulin, cAMP, and pten gene deletion. J. Neurosci. 2010, 30:15654-15663.
37. Lai J.P., Dalton J.T., Knoell D.L. Phosphatase and tensin homologue deleted on chromosome ten (PTEN) as a molecular target in lung epithelial wound repair. Br. J. Pharmacol. 2007, 152:1172-1184.
38. Lee J.K., Kim J.E., Sivula M., Strittmatter S.M. Nogo receptor antagonism promotes stroke recovery by enhancing axonal plasticity. J. Neurosci. 2004, 24:6209-6217.
39. Lee H., McKeon R.J., Bellamkonda R.V. Sustained delivery of thermostabilized chABC enhances axonal sprouting and functional recovery after spinal cord injury. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:3340-3345.
40. Leon S., Yin Y., Nguyen J., Irwin N., Benowitz L.I. Lens injury stimulates axon regeneration in the mature rat optic nerve. J. Neurosci. 2000, 20:4615-4626.
41. Li S., Liu B.P., Budel S., Li M., Ji B., Walus L., Li W., Jirik A., Rabacchi S., Choi E., Worley D., Sah D.W., Pepinsky B., Lee D., Relton J., Strittmatter S.M. Blockade of Nogo-66, myelin-associated glycoprotein, and oligodendrocyte myelin glycoprotein by soluble Nogo-66 receptor promotes axonal sprouting and recovery after spinal injury. J. Neurosci. 2004, 24:10511-10520.
42. Liu K., Lu Y., Lee J.K., Samara R., Willenberg R., Sears-Kraxberger I., Tedeschi A., Park K.K., Jin D., Cai B., Xu B., Connolly L., Steward O., Zheng B., He Z. PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat. Neurosci. 2010, 13:1075-1081.
43. Low K., Culbertson M., Bradke F., Tessier-Lavigne M., Tuszynski M.H. Netrin-1 is a novel myelin-associated inhibitor to axon growth. J. Neurosci. 2008, 28:1099-1108.
44. MacDermid V.E., McPhail L.T., Tsang B., Rosenthal A., Davies A., Ramer M.S. A soluble Nogo receptor differentially affects plasticity of spinally projecting axons. Eur. J. Neurosci. 2004, 20:2567-2579.
45. 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.
46. Massey J.M., Amps J., Viapiano M.S., Matthews R.T., Wagoner M.R., Whitaker C.M., Alilain W., Yonkof A.L., Khalyfa A., Cooper N.G., Silver J., Onifer S.M. Increased chondroitin sulfate proteoglycan expression in denervated brainstem targets following spinal cord injury creates a barrier to axonal regeneration overcome by chondroitinase ABC and neurotrophin-3. Exp. Neurol. 2008, 209:426-445.
47. 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.
48. 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.
49. Mitsui T., Fischer I., Shumsky J.S., Murray M. Transplants of fibroblasts expressing BDNF and NT-3 promote recovery of bladder and hindlimb function following spinal contusion injury in rats. Exp. Neurol. 2005, 194:410-431.
50. 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.
51. Nakashima S., Arnold S.A., Mahoney E.T., Sithu S.D., Zhang Y.P., D'Souza S.E., Shields C.B., Hagg T. Small-molecule protein tyrosine phosphatase inhibition as a neuroprotective treatment after spinal cord injury in adult rats. J. Neurosci. 2008, 28:7293-7303.
52. Neumann S., Woolf C.J. Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron 1999, 23:83-91.
53. Oudega M., Rosano C., Sadi D., Wood P.M., Schwab M.E., Hagg T. Neutralizing antibodies against neurite growth inhibitor NI-35/250 do not promote regeneration of sensory axons in the adult rat spinal cord. Neuroscience 2000, 100:873-883.
54. Park K.K., Liu K., Hu Y., Smith P.D., Wang C., Cai B., Xu B., Connolly L., Kramvis I., Sahin M., He Z. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 2008, 322:963-966.
55. Pizzorusso T., Medini P., Berardi N., Chierzi S., Fawcett J.W., Maffei L. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 2002, 298:1248-1251.
56. Raineteau O., Fouad K., Bareyre F.M., Schwab M.E. Reorganization of descending motor tracts in the rat spinal cord. Eur. J. Neurosci. 2002, 16:1761-1771.
57. Richardson P.M., Issa V.M. Peripheral injury enhances central regeneration of primary sensory neurones. Nature 1984, 309:791-793.
58. Richardson P.M., McGuinness U.M., Aguayo A.J. Axons from CNS neurons regenerate into PNS grafts. Nature 1980, 284:264-265.
59. Robak L.A., Venkatesh K., Lee H., Raiker S.J., Duan Y., Lee-Osbourne J., Hofer T., Mage R.G., Rader C., Giger R.J. Molecular basis of the interactions of the Nogo-66 receptor and its homolog NgR2 with myelin-associated glycoprotein: development of NgROMNI-Fc, a novel antagonist of CNS myelin inhibition. J. Neurosci. 2009, 29:5768-5783.
60. Runker A.E., Little G.E., Suto F., Fujisawa H., Mitchell K.J. Semaphorin-6A controls guidance of corticospinal tract axons at multiple choice points. Neural Dev. 2008, 3:34.
61. Schnell L., Schneider R., Kolbeck R., Barde Y.A., Schwab M.E. Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 1994, 367:170-173.
62. Schwab J.M., Conrad S., Monnier P.P., Julien S., Mueller B.K., Schluesener H.J. Spinal cord injury-induced lesional expression of the repulsive guidance molecule (RGM). Eur. J. Neurosci. 2005, 21:1569-1576.
63. Skene J.H. Axonal growth-associated proteins. Annu. Rev. Neurosci. 1989, 12:127-156.
64. Snow D.M., Lemmon V., Carrino D.A., Caplan A.I., Silver J. Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp. Neurol. 1990, 109:111-130.
65. Steinmetz M.P., Horn K.P., Tom V.J., Miller J.H., Busch S.A., Nair D., Silver D.J., Silver J. Chronic enhancement of the intrinsic growth capacity of sensory neurons combined with the degradation of inhibitory proteoglycans allows functional regeneration of sensory axons through the dorsal root entry zone in the mammalian spinal cord. J. Neurosci. 2005, 25:8066-8076.
66. Thuret S., Moon L.D., Gage F.H. Therapeutic interventions after spinal cord injury. Nat. Rev. Neurosci. 2006, 7:628-643.
67. Tobias C.A., Shumsky J.S., Shibata M., Tuszynski M.H., Fischer I., Tessler A., Murray M. Delayed grafting of BDNF and NT-3 producing fibroblasts into the injured spinal cord stimulates sprouting, partially rescues axotomized red nucleus neurons from loss and atrophy, and provides limited regeneration. Exp. Neurol. 2003, 184:97-113.
68. Tuszynski M.H., Grill R., Jones L.L., Brant A., Blesch A., Low K., Lacroix S., Lu P. NT-3 gene delivery elicits growth of chronically injured corticospinal axons and modestly improves functional deficits after chronic scar resection. Exp. Neurol. 2003, 181:47-56.
69. Venkatesh K., Chivatakarn O., Lee H., Joshi P.S., Kantor D.B., Newman B.A., Mage R., Rader C., Giger R.J. The Nogo-66 receptor homolog NgR2 is a sialic acid-dependent receptor selective for myelin-associated glycoprotein. J. Neurosci. 2005, 25:808-822.
70. 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.
71. Wang X., Chun S.-J., Treloar H., Vartanian T., Greer C.A., Strittmatter S.M. Localization of Nogo-A and Nogo-66 receptor proteins at sites of axon-myelin and synaptic contact. J. Neurosci. 2002, 22:5505-5515.
72. Wang X., Baughman K.W., Basso D.M., Strittmatter S.M. Delayed Nogo receptor therapy improves recovery from spinal cord contusion. Ann. Neurol. 2006, 60:540-549.
73. Wang X., Duffy P., McGee A.W., Hasan O., Gould G., Tu N., Harel N.Y., Huang Y., Carson R.D., Weinzimmer D., Ropchan J., Benowitz L.I., Cafferty W.B.J., Strittmatter S.M. Recovery from chronic spinal cord contusion after Nogo receptor intervention. Ann. Neurol. 2011, 70:805-821.
74. Ye J.H., Houle J.D. Treatment of the chronically injured spinal cord with neurotrophic factors can promote axonal regeneration from supraspinal neurons. Exp. Neurol. 1997, 143:70-81.
75. Yin Y., Cui Q., Li Y., Irwin N., Fischer D., Harvey A.R., Benowitz L.I. Macrophage-derived factors stimulate optic nerve regeneration. J. Neurosci. 2003, 23:2284-2293.
76. Yin Y., Henzl M.T., Lorber B., Nakazawa T., Thomas T.T., Jiang F., Langer R., Benowitz L.I. Oncomodulin is a macrophage-derived signal for axon regeneration in retinal ganglion cells. Nat. Neurosci. 2006, 9:843-852.
77. Yin Y., Cui Q., Gilbert H.Y., Yang Y., Yang Z., Berlinicke C., Li Z., Zaverucha-do-Valle C., He H., Petkova V., Zack D.J., Benowitz L.I. Oncomodulin links inflammation to optic nerve regeneration. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:19587-19592.
78. Zai L., Ferrari C., Dice C., Subbaiah S., Havton L.A., Coppola G., Geschwind D., Irwin N., Huebner E., Strittmatter S.M., Benowitz L.I. Inosine augments the effects of a Nogo receptor blocker and of environmental enrichment to restore skilled forelimb use after stroke. J. Neurosci. 2011, 31:834-843.
79. Zheng B., Atwal J., Ho C., Case L., He X.L., Garcia K.C., Steward O., Tessier-Lavigne M. Genetic deletion of the Nogo receptor does not reduce neurite inhibition in vitro or promote corticospinal tract regeneration in vivo. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:1205-1210.