Construction of pathways to promote axon growth within the adult central nervous system

Brain Research Bulletin

Volumn 84, Issue 4-5, 2011, Pages 300-305

  Smith, George M ^a   Onifer, Stephen M ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Axon regeneration; Gradient; Guidance molecules; Neurotrophin; Spinal cord injury

Indexed keywords

NERVE GROWTH FACTOR; NEUROTROPHIN;

CELL TRANSPLANTATION; CENTRAL NERVOUS SYSTEM; HUMAN; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SCHWANN CELL; SIGNAL TRANSDUCTION; SPINAL CORD INJURY;

AXONS; CELL TRANSPLANTATION; CENTRAL NERVOUS SYSTEM; NERVE GROWTH FACTORS; NERVE REGENERATION; SPINAL CORD INJURIES;

EID: 79951772161     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2010.05.013     Document Type: Review

References (87)

1. Alto L.T., Havton L.A., Conner J.M., Hollis Ii E.R., Blesch A., Tuszynski M.H. Hemotropic guidance facilitates axonal regeneration and synapse formation after spinal cord injury. Nat. Neurosci. 2009, 12:1106-1113.
2. Andrews M.R., Stelzner D.J. Evaluation of olfactory ensheathing and Schwann cells after implantation into a dorsal injury of adult rat spinal cord. J. Neurotrauma 2007, 24:1773-1792.
3. Bamber N.I., Li H.Y., Aebischer P., Xu X.M. Fetal spinal cord tissue in guidance channels promotes longitudinal axonal growth in the partially lesioned adult rat spinal cord. Neural Plast. 1999, 6:103-121.
4. Bamber N.I., Li H., Lu X., Oudega M., Aebischer P., Xu X.M. Neurotrophins BDNF and NT-3 promote axonal re-entry into the distal host spinal cord through Schwann cell-seeded mini-channels. Eur. J. Neurosci. 2001, 13:257-268.
5. Bernstein J.J., Goldberg W.J. Fetal spinal cord homografts ameliorate the severity of lesion-induced hind limb behavioral deficits. Exp. Neurol. 1987, 98:633-644.
6. Blesch A., Tuszynski M.H. Transient growth factor delivery sustains regenerated axons after spinal cord injury. J. Neurosci. 2007, 27:10535-10545.
7. Blits B., Oudega M., Boer G.J., Bartlett Bunge M., Verhaagen J. Adeno-associated viral vector-mediated neurotrophin gene transfer in the injured adult rat spinal cord improves hind-limb function. Neuroscience 2003, 118:271-281.
8. Bonner J.F., Blesch A., Neuhuber B., Fischer I. Promoting directional axon growth from neural progenitors grafted into the injured spinal cord. J. Neurosci. Res. 2009.
9. Bregman B.S., Kunkel-Bagden E., Reier P.J., Dai H.N., McAtee M., Gao D. 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. 1993, 123:3-16.
10. Cameron A.A., Smith G.M., Randall D.C., Brown D.R., Rabchevsky A.G. Genetic manipulation of intraspinal plasticity after spinal cord injury alters the severity of autonomic dysreflexia. J. Neurosci. 2006, 26:2923-2932.
11. Chau C.H., Shum D.K., Li H., Pei J., Lui Y.Y., Wirthlin L., Chan Y.S., Xu X.M. Chondroitinase ABC enhances axonal regrowth through Schwann cell-seeded guidance channels after spinal cord injury. Faseb J. 2004, 18:194-196.
12. Cheng H., Cao Y., Olson L. Spinal cord repair in adult paraplegic rats: partial restoration of hind limb function. Science 1996, 273:510-513.
13. Cheng H., Liao K.K., Liao S.F., Chuang T.Y., Shih Y.H. Spinal cord repair with acidic fibroblast growth factor as a treatment for a patient with chronic paraplegia. Spine 2004, 29:E284-288.
14. Chuah M.I., Choi-Lundberg D., Weston S., Vincent A.J., Chung R.S., Vickers J.C., West A.K. Olfactory ensheathing cells promote collateral axonal branching in the injured adult rat spinal cord. Exp. Neurol. 2004, 185:15-25.
15. Coumans J.V., Lin T.T., Dai H.N., MacArthur L., McAtee M., Nash C., Bregman B.S. Axonal regeneration and functional recovery after complete spinal cord transection in rats by delayed treatment with transplants and neurotrophins. J. Neurosci. 2001, 21:9334-9344.
16. Curinga G., Smith G.M. Molecular/genetic manipulation of extrinsic axon guidance factors for CNS repair and regeneration. Exp. Neurol. 2008, 209:333-342.
17. Davies S.J., Fitch M.T., Memberg S.P., Hall A.K., Raisman G., Silver J. Regeneration of adult axons in white matter tracts of the central nervous system. Nature 1997, 390:680-683.
18. Davies S.J., 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.
19. Dobkin B.H., Curt A., Guest J. Cellular transplants in China: observational study from the largest human experiment in chronic spinal cord injury. Neurorehabil. Neural Repair 2006, 20:5-13.
20. Dontchev V.D., Letourneau PC Nerve growth factor and semaphorin 3A signaling pathways interact in regulating sensory neuronal growth cone motility. J. Neurosci. 2002, 22:6659-6669.
21. Falci S., Holtz A., Akesson E., Azizi M., Ertzgaard P., Hultling C., Kjaeldgaard A., Levi R., Ringden O., Westgren M., Lammertse D., Seiger A. Obliteration of a posttraumatic spinal cord cyst with solid human embryonic spinal cord grafts: first clinical attempt. J. Neurotrauma 1997, 14:875-884.
22. Fouad K., Schnell L., Bunge M.B., Schwab M.E., Liebscher T., Pearse D.D. Combining Schwann cell bridges and olfactory-ensheathing glia grafts with chondroitinase promotes locomotor recovery after complete transection of the spinal cord. J. Neurosci. 2005, 25:1169-1178.
23. Fraidakis M.J., Spenger C., Olson L. Partial recovery after treatment of chronic paraplegia in rat. Exp. Neurol. 2004, 188:33-42.
24. Gaillard A., Prestoz L., Dumartin B., Cantereau A., Morel F., Roger M., Jaber M. Reestablishment of damaged adult motor pathways by grafted embryonic cortical neurons. Nat. Neurosci. 2007, 10:1294-1299.
25. Golden K.L., Pearse D.D., Blits B., Garg M.S., Oudega M., Wood P.M., Bunge M.B. Transduced Schwann cells promote axon growth and myelination after spinal cord injury. Exp. Neurol. 2007, 207:203-217.
26. Guest J.D., Hesse D., Schnell L., Schwab M.E., Bunge M.B., Bunge R.P. Influence of IN-1 antibody and acidic FGF-fibrin glue on the response of injured corticospinal tract axons to human Schwann cell grafts. J. Neurosci. Res. 1997, 50:888-905.
27. Guest J.D., Herrera L.P., Qian T. Rapid recovery of segmental neurological function in a tetraplegic patient following transplantation of fetal olfactory bulb-derived cells. Spinal Cord 2006, 44:135-142.
28. Hofstetter C.P., Schwarz E.J., Hess D., Widenfalk J., El Manira A., Prockop D.J., Olson L. Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:2199-2204.
29. Houle J.D., Tom V.J., Mayes D., Wagoner G., Phillips N., Silver J. Combining an autologous peripheral nervous system "bridge" and matrix modification by chondroitinase allows robust, functional regeneration beyond a hemisection lesion of the adult rat spinal cord. J. Neurosci. 2006, 26:7405-7415.
30. Hu X., Cai J., Yang J., Smith G.M. Sensory axon targeting is increased by NGF gene therapy within the lesioned adult femoral nerve. Exp. Neurol. 2009.
31. Huang H., Chen L., Xi H., Wang Q., Zhang J., Liu Y., Zhang F. Olfactory ensheathing cells transplantation for central nervous system diseases in 1,255 patients. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 2009, 23:14-20.
32. Iannotti C., Li H., Yan P., Lu X., Wirthlin L., Xu X.-M. Glial cell line-derived neurotrophic factor-enriched bridging transplants promote propriospinal axonal regeneration and enhance myelination after spinal cord injury. Exp. Neurol. 2003, 183:379-393.
33. Jeffery N.D., Lakatos A., Franklin R.J. Autologous olfactory glial cell transplantation is reliable and safe in naturally occurring canine spinal cord injury. J. Neurotrauma 2005, 22:1282-1293.
34. Jin Y., Ziemba K.S., Smith G.M. Axon growth across a lesion site along a preformed guidance pathway in the brain. Exp. Neurol. 2008, 210:521-530.
35. 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.
36. Kalincík T., Choi E.A., Féron F., Bianco J., Sutharsan R., Hayward I., Mackay-Sim A., Carrive P., Waite P.M. Olfactory ensheathing cells reduce duration of autonomic dysreflexia in rats with high spinal cord injury. Auton. Neurosci. 2009, (Epub ahead of print).
37. Keyvan-Fouladi N., Raisman G., Li Y. Functional repair of the corticospinal tract by delayed transplantation of olfactory ensheathing cells in adult rats. J. Neurosci. 2003, 23:9428-9434.
38. Kim B.G., Dai H.N., Lynskey J.V., McAtee M., Bregman B.S. Degradation of chondroitin sulfate proteoglycans potentiates transplant-mediated axonal remodeling and functional recovery after spinal cord injury in adult rats. J. Comp. Neurol. 2006, 497:182-198.
39. Levi A.D., Dancausse H., Li X., Duncan S., Horkey L., Oliviera M. Peripheral nerve grafts promoting central nervous system regeneration after spinal cord injury in the primate. J. Neurosurg. 2002, 96:197-205.
40. Li L., Field P.M., Raisman G. Repair of adult rat corticospinal tract by transplants of olfactory ensheathing cells. Science 1997, 277:2000-2002.
41. Li Y., Decherchi P., Raisman G. Transplantation of olfactory ensheathing cells into spinal cord lesions restores breathing and climbing. J. Neurosci. 2003, 23:727-731.
42. Lima C., Pratas-Vital J., Escada P., Hasse-Ferreira A., Capucho C., Peduzzi J.D. Olfactory mucosa autografts in human spinal cord injury: a pilot clinical study. J. Spinal Cord Med. 2006, 29:191-203.
43. Lu P., Yang H., Jones L.L., Filbin M.T., Tuszynski M.H. Combinatorial therapy with neurotrophins and cAMP promotes axonal regeneration beyond sites of spinal cord injury. J. Neurosci. 2004, 24:6402-6409.
44. Lynskey J.V., Sandhu F.A., Dai H.N., McAtee M., Slotkin J.R., MacArthur L., Bregman B.S. Delayed intervention with transplants and neurotrophic factors supports recovery of forelimb function after cervical spinal cord injury in adult rats. J. Neurotrauma 2006, 23:617-634.
45. Mackay-Sim A., Feron F., Cochrane J., Bassingthwaighte L., Bayliss C., Davies W., Fronek P., Gray C., Kerr G., Licina P., Nowitzke A., Perry C., Silburn P.A., Urquhart S., Geraghty T. Autologous olfactory ensheathing cell transplantation in human paraplegia: a 3-year clinical trial. Brain 2008, 131:2376-2386.
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. Menei P., Montero-Menei C., Whittemore S.R., Bunge R.P., Bunge M.B. Schwann cells genetically modified to secrete human BDNF promote enhanced axonal regrowth across transected adult rat spinal cord. Eur. J. Neurosci. 1998, 10:607-621.
48. Messersmith E.K., Leonardo E.D., Shatz C.J., Tessier-Lavigne M., Goodman C.S., Kolodkin A.L. Semaphorin III can function as a selective chemorepellent to pattern sensory projections in the spinal cord. Neuron 1995, 14::949-959.
49. 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.
50. Nikulina E., Tidwell J.L., Dai H.N., Bregman B.S., Filbin M.T. The phosphodiesterase inhibitor rolipram delivered after a spinal cord lesion promotes axonal regeneration and functional recovery. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:8786-8790.
51. Oudega M., Gautier S.E., Chapon P., Fragoso M., Bates M.L., Parel J.M., Bunge M.B. Axonal regeneration into Schwann cell grafts within resorbable poly(alpha-hydroxyacid) guidance channels in the adult rat spinal cord. Biomaterials 2001, 22:1125-1136.
52. Oudega M., Hagg T. Nerve growth factor promotes regeneration of sensory axons into adult rat spinal cord. Exp. Neurol. 1996, 140:218-229.
53. Oudega M., Hagg T. Neurotrophins promote regeneration of sensory axons in the adult rat spinal cord. Brain Res. 1999, 818:431-438.
54. Pearse D.D., Pereira F.C., Marcillo A.E., Bates M.L., Berrocal Y.A., Filbin M.T., Bunge M.B. cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat. Med. 2004, 10:610-616.
55. Ramer L.M., Au E., Richter M.W., Liu J., Tetzlaff W., Roskams A.J. Peripheral olfactory ensheathing cells reduce scar and cavity formation and promote regeneration after spinal cord injury. J. Comp. Neurol. 2004, 473:1-15.
56. Ramon y Cajal S. Degeneration and Regeneration of the Nervous System 1928, Hafner, New York.
57. Ramón-Cueto A., Cordero M.I., Santos-Benito F.F., Avila J. Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 2000, 25:425-435.
58. Ramón-Cueto A., Plant G.W., Avila J., Bunge M.B. Long-distance axonal regeneration in the transected adult rat spinal cord is promoted by olfactory ensheathing glia transplants. J. Neurosci. 1998, 18:3803-3815.
59. Reier P.J., Stokes B.T., Thompson F.J., Anderson D.K. Fetal cell grafts into resection and contusion/compression injuries of the rat and cat spinal cord. Exp. Neurol. 1992, 115:177-188.
60. Richardson P.M., McGuinness U.M., Aguayo A.J. Axons from CNS neurones regenerate into PNS grafts. Nature 1980, 284:264-265.
61. Richardson P.M., McGuinness U.M., Aguayo A.J. Peripheral nerve autografts to the rat spinal cord: studies with axonal tracing methods. Brain Res. 1982, 237:147-162.
62. Richter M.W., Fletcher P.A., Liu J., Tetzlaff W., Roskams A.J. Lamina propria and olfactory bulb ensheathing cells exhibit differential integration and migration and promote differential axon sprouting in the lesioned spinal cord. J. Neurosci. 2005, 25:10700-10711.
63. Rochkind S., Shahar A., Fliss D., El-Ani D., Astachov L., Hayon T., Alon M., Zamostiano R., Ayalon O., Biton I.E., Cohen Y., Halperin R., Schneider D., Oron A., Nevo Z. Development of a tissue-engineered composite implant for treating traumatic paraplegia in rats. Eur. Spine J. 2006, 15:234-245.
64. Romero M.I., Rangappa N., Li L., Lightfoot E., Garry M.G., Smith G.M. Extensive sprouting of sensory afferents and hyperalgesia induced by conditional expression of nerve growth factor in the adult spinal cord. J. Neurosci. 2000, 20:4435-4445.
65. Romero M.I., Rangappa N., Garry M.G., Smith G.M. Functional regeneration of chronically injured sensory afferents into adult spinal cord after neurotrophin gene therapy. J. Neurosci. 2001, 21:8408-8416.
66. Saberi H., Moshayedi P., Aghayan H.R., Arjmand B., Hosseini S.K., Emami-Razavi S.H., Rahimi-Movaghar V., Raza M., Firouzi M. Treatment of chronic thoracic spinal cord injury patients with autologous Schwann cell transplantation: an interim report on safety considerations and possible outcomes. Neurosci. Lett. 2008, 443:46-50.
67. Sasaki M., Lankford K.L., Zemedkun M., Kocsis J.D. Identified olfactory ensheathing cells transplanted into the transected dorsal funiculus bridge the lesion and form myelin. J. Neurosci. 2004, 24:8485-8493.
68. Silver J., Miller J.H. Regeneration beyond the glial scar. Nat. Rev. Neurosci. 2004, 5(2):146-156.
69. Song H.J., Poo M.M. Signal transduction underlying growth cone guidance by diffusible factors. Curr. Opin. Neurobiol. 1999, 9:355-363.
70. Spencer T., Filbin M.T. A role for cAMP in regeneration of the adult mammalian CNS. J. Anat. 2004, 204:49-55.
71. Sperry R.W. Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc. Natl. Acad. Sci. U.S.A. 1963, 50:703-710.
72. Tang X.Q., Tanelian D.L., Smith G.M. Semaphorin3A inhibits nerve growth factor-induced sprouting of nociceptive afferents in adult rat spinal cord. J. Neurosci. 2004, 24:819-827.
73. Tang X.Q., Cai J., Nelson K.D., Peng X.J., Smith G.M. Functional repair after dorsal root rhizotomy using nerve conduits and neurotrophic molecules. Eur. J. Neurosci. 2004, 20:1211-1218.
74. Tang X.Q., Heron P., Mashburn C., Smith G.M. Targeting sensory axon regeneration in adult spinal cord. J. Neurosci. 2007, 27:6068-6078.
75. Taylor L., Jones L., Tuszynski M.H., Blesch A. Neurotrophin-3 gradients established by lentiviral gene delivery promote short-distance axonal bridging beyond cellular grafts in the injured spinal cord. J. Neurosci. 2006, 26:9713-9721.
76. Tessier-Lavigne M., Goodman C.S. The molecular biology of axon guidance. Science 1996, 274:1123-1133.
77. Thompson L.H., Grealish S., Kirik D., Björklund A. Reconstruction of the nigrostriatal dopamine pathway in the adult mouse brain. Eur. J. Neurosci. 2009, 30:625-638.
78. Vavrek R., Pearse D.D., Fouad K. Neuronal populations capable of regeneration following a combined treatment in rats with spinal cord transection. J. Neurotrauma 2007, 24:1667-1673.
79. Wang R., King T., Ossipov M.H., Rossomando A.J., Vanderah T.W., Harvey P., Cariani P., Frank E., Sah D.W., Porreca F. Persistent restoration of sensory function by immediate or delayed systemic artemin after dorsal root injury. Nat. Neurosci. 2008, 11:488-496.
80. Wirth E.D., Reier P.J., Fessler R.G., Thompson F.J., Uthman B., Behrman A., Beard J., Vierck C.J., Anderson D.K. Feasibility and safety of neural tissue transplantation in patients with syringomyelia. J. Neurotrauma 2001, 18:911-929.
81. Wright D.E., White F.A., Gerfen R.W., Silos-Santiago I., Snider W.D. The guidance molecule semaphorin III is expressed in regions of spinal cord and periphery avoided by growing sensory axons. J. Comp. Neurol. 1995, 361(October (2)):321-333.
82. Xu X.M., Onifer S.M. Transplantation-mediated strategies to promote axonal regeneration following spinal cord injury. Respir. Physiol. Neurobiol. 2009, 169:171-182.
83. Xu X.M., Guenard V., Kleitman N., Aebischer P., Bunge M.B. A combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schwann cell grafts in adult rat thoracic spinal cord. Exp. Neurol. 1995, 134:261-272.
84. Yoon S.H., Shim Y.S., Park Y.H., Chung J.K., Nam J.H., Kim M.O., Park H.C., Park S.R., Min B.H., Kim E.Y., Choi B.H., Park H., Ha Y. Complete spinal cord injury treatment using autologous bone marrow cell transplantation and bone marrow stimulation with granulocyte macrophage-colony stimulating factor: phase I/II clinical trial. Stem Cells 2007, 25:2066-2073.
85. Zhang L., Ma Z., Smith G.M., Wen X., Pressman Y., Wood P.M., Xu X.M. GDNF-enhanced axonal regeneration and myelination following spinal cord injury is mediated by primary effects on neurons. Glia 2009, 57:1178-1191.
86. Zhang Y., Dijkhuizen P.A., Anderson P.N., Lieberman A.R., Verhaagen J. NT-3 delivered by an adenoviral vector induces injured dorsal root axons to regenerate into the spinal cord of adult rats. J. Neurosci. Res. 1998, 54:554-562.
87. Ziemba K., Chaudhry N., Rabchevsky A.G., Jin Y., Smith G.M. Targeting axon growth from neuronal transplants along preformed guidance pathways in the adult central nervous system. J. Neurosci. 2008, 28:340-348.