From microsurgery to nanosurgery: how viral vectors may help repair the peripheral nerve

Progress in Brain Research

Volumn 175, Issue , 2009, Pages 173-186

  Tannemaat, Martijn R ^a,b   Boer, Gerard J ^a   Eggers, Ruben ^a   Malessy, Martijn J A ^b   Verhaagen, Joost ^a  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

gene therapy; neurotrophic factors; peripheral nerve; regeneration; viral vectors

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; LENTIVIRUS VECTOR; PARVOVIRUS VECTOR; VIRUS VECTOR;

CELL SURVIVAL; GENE OVEREXPRESSION; GENE THERAPY; HUMAN; MICROSURGERY; MOTONEURON; NANOSURGERY; NERVE FIBER GROWTH; NERVE GRAFT; NERVE REGENERATION; NEUROSURGERY; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

ANIMALS; GENE THERAPY; GENETIC VECTORS; HUMANS; MICROSURGERY; NANOTECHNOLOGY; NERVE REGENERATION; PERIPHERAL NERVES;

EID: 67949084778     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0079-6123(09)17512-X     Document Type: Review

References (80)

1. Ara J., Bannerman P., Hahn A., Ramirez S., and Pleasure D. Modulation of sciatic nerve expression of class 3 semaphorins by nerve injury. Neurochemical Research 29 (2004) 1153-1159
2. Badalamente M.A., Hurst L.C., Ellstein J., and McDevitt C.A. The pathobiology of human neuromas: An electron microscopic and biochemical study. Journal of Hand Surgery [British Volume] 10 (1985) 49-53
3. Beard B.C., Dickerson D., Beebe K., Gooch C., Fletcher J., Okbinoglu T., et al. Comparison of HIV-derived lentiviral and MLV-based gammaretroviral vector integration sites in primate repopulating cells. Molecular Therapy 15 (2007) 1356-1365
4. Blesch A., Conner J., Pfeifer A., Gasmi M., Ramirez A., Britton W., et al. Regulated lentiviral NGF gene transfer controls rescue of medial septal cholinergic neurons. Molecular Therapy 11 (2005) 916-925
5. Blesch A., and Tuszynski M.H. Transient growth factor delivery sustains regenerated axons after spinal cord injury. Journal of Neuroscience 27 (2007) 10535-10545
6. Blits B., Carlstedt T.P., Ruitenberg M.J., de Winter F., Hermens W.T., Dijkhuizen P.A., et al. Rescue and sprouting of motoneurons following ventral root avulsion and reimplantation combined with intraspinal adeno-associated viral vector-mediated expression of glial cell line-derived neurotrophic factor or brain-derived neurotrophic factor. Experimental Neurology 189 (2004) 303-316
7. Bosse F., Hasenpusch-Theil K., Kury P., and Muller H.W. Gene expression profiling reveals that peripheral nerve regeneration is a consequence of both novel injury-dependent and reactivated developmental processes. Journal of Neurochemistry 96 (2006) 1441-1457
8. Boyd J.G., and Gordon T. A dose-dependent facilitation and inhibition of peripheral nerve regeneration by brain-derived neurotrophic factor. European Journal of Neuroscience 15 (2002) 613-626
9. Boyd J.G., and Gordon T. Glial cell line-derived neurotrophic factor and brain-derived neurotrophic factor sustain the axonal regeneration of chronically axotomized motoneurons in vivo. Experimental Neurology 183 (2003) 610-619
10. Boyd J.G., and Gordon T. Neurotrophic factors and their receptors in axonal regeneration and functional recovery after peripheral nerve injury. Molecular Neurobiology 27 (2003) 277-324
11. Bozkurt A., Brook G.A., Moellers S., Lassner F., Sellhaus B., Weis J., et al. In vitro assessment of axonal growth using dorsal root ganglia explants in a novel three-dimensional collagen matrix. Tissue Engineering 13 (2007) 2971-2979
12. Brushart T.M. Motor axons preferentially reinnervate motor pathways. Journal of Neuroscience 13 (1993) 2730-2738
13. Burstyn-Cohen T., Frumkin A., Xu Y.T., Scherer S.S., and Klar A. Accumulation of F-spondin in injured peripheral nerve promotes the outgrowth of sensory axons. Journal of Neuroscience 18 (1998) 8875-8885
14. Carter B.J. Adeno-associated virus vectors in clinical trials. Human Gene Therapy 16 (2005) 541-550
15. Cattoglio C., Facchini G., Sartori D., Antonelli A., Miccio A., Cassani B., et al. Hot spots of retroviral integration in human CD34+ hematopoietic cells. Blood 110 (2007) 1770-1778
16. Chen Z.L., Yu W.M., and Strickland S. Peripheral regeneration. Annual Review of Neuroscience 30 (2007) 209-233
17. Clarke H.M., and Curtis C.G. An approach to obstetrical brachial plexus injuries. Hand Clinics 11 (1995) 563-580 Discussion pp. 580-561.
18. DeMatteo C., Bain J.R., Galea V., and Gjertsen D. Botulinum toxin as an adjunct to motor learning therapy and surgery for obstetrical brachial plexus injury. Developmental Medicine and Child Neurology 48 (2006) 245-252
19. de Ruiter G.C., Malessy M.J., Alaid A.O., Spinner R.J., Engelstad J.K., Sorenson E.J., et al. Misdirection of regenerating motor axons after nerve injury and repair in the rat sciatic nerve model. Experimental Neurology 211 (2008) 339-350
20. de Ruiter G.C., Onyeneho I.A., Liang E.T., Moore M.J., Knight A.M., Malessy M.J., et al. Methods for in vitro characterization of multichannel nerve tubes. Journal of Biomedical Materials Research A 84 (2008) 643-651
21. Eberhardt K.A., Irintchev A., Al-Majed A.A., Simova O., Brushart T.M., Gordon T., et al. BDNF/TrkB signaling regulates HNK-1 carbohydrate expression in regenerating motor nerves and promotes functional recovery after peripheral nerve repair. Experimental Neurology 198 (2006) 500-510
22. Eggers R., Hendriks W.T., Tannemaat M.R., van Heerikhuize J.J., Pool C.W., Carlstedt T.P., et al. Neuroregenerative effects of lentiviral vector-mediated GDNF expression in reimplanted ventral roots. Molecular and Cellular Neuroscience 39 (2008) 105-117
23. Elsworth J.D., Redmond Jr. D.E., Leranth C., Bjugstad K.B., Sladek Jr. J.R., Collier T.J., et al. AAV2-mediated gene transfer of GDNF to the striatum of MPTP monkeys enhances the survival and outgrowth of co-implanted fetal dopamine neurons. Experimental Neurology 211 (2008) 252-258
24. Fine E.G., Decosterd I., Papaloizos M., Zurn A.D., and Aebischer P. GDNF and NGF released by synthetic guidance channels support sciatic nerve regeneration across a long gap. European Journal of Neuroscience 15 (2002) 589-601
25. Fu S.Y., and Gordon T. Contributing factors to poor functional recovery after delayed nerve repair: prolonged denervation. Journal of Neuroscience 15 (1995) 3886-3895
26. Fu S.Y., and Gordon T. Contributing factors to poor functional recovery after delayed nerve repair: Prolonged axotomy. Journal of Neuroscience 15 (1995) 3876-3885
27. Furey M.J., Midha R., Xu Q.G., Belkas J., and Gordon T. Prolonged target deprivation reduces the capacity of injured motoneurons to regenerate. Neurosurgery 60 (2007) 723-732 Discussion pp. 732-723.
28. Galtrey C.M., Asher R.A., Nothias F., and Fawcett J.W. Promoting plasticity in the spinal cord with chondroitinase improves functional recovery after peripheral nerve repair. Brain 130 (2007) 926-939
29. Gilbert A., and Tassin J.L. Surgical repair of the brachial plexus in obstetric paralysis. Chirurgie 110 (1984) 70-75
30. Gossen M., and Bujard H. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proceedings of the National Academy of Science USA 89 (1992) 5547-5551
31. Gramsbergen A., IJkema-Paassen J., and Meek M.F. Sciatic nerve transection in the adult rat: Abnormal EMG patterns during locomotion by aberrant innervation of hindleg muscles. Experimental Neurology 161 (2000) 183-193
32. Hargrove P.W., Kepes S., Hanawa H., Obenauer J.C., Pei D., Cheng C., et al. Globin lentiviral vector insertions can perturb the expression of endogenous genes in beta-thalassemic hematopoietic cells. Molecular Therapy 16 (2008) 525-533
33. Hattori T., Matsuyama Y., Sakai Y., Ishiguro N., Hirata H., and Nakamura R. Chondrotinase ABC enhances axonal regeneration across nerve gaps. Journal of Clinical Neuroscience 15 (2008) 185-191
34. Helgren M.E., Squinto S.P., Davis H.L., Parry D.J., Boulton T.G., Heck C.S., et al. Trophic effect of ciliary neurotrophic factor on denervated skeletal muscle. Cell 76 (1994) 493-504
35. Hendriks W.T., Eggers R., Carlstedt T.P., Zaldumbide A., Tannemaat M.R., Fallaux F.J., et al. Lentiviral vector-mediated reporter gene expression in avulsed spinal ventral root is short-term, but is prolonged using an immune "stealth" transgene. Restorative Neurology and Neuroscience 25 (2007) 585-599
36. Hoke A. Mechanisms of disease: What factors limit the success of peripheral nerve regeneration in humans?. Natural Clinical Practices in Neurology 2 (2006) 448-454
37. Hoke A., Redett R., Hameed H., Jari R., Zhou C., Li Z.B., et al. Schwann cells express motor and sensory phenotypes that regulate axon regeneration. Journal of Neuroscience 26 (2006) 9646-9655
38. Huang S., Wang F., Hong G., Wan S., and Kang H. Protective effects of ciliary neurotrophic factor on denervated skeletal muscle. Journal of Huazhong University of Science Technology and Medical Science 22 (2002) 148-151
39. Huber A.B., Kania A., Tran T.S., Gu C., De Marco Garcia N., Lieberam I., et al. Distinct roles for secreted semaphorin signaling in spinal motor axon guidance. Neuron 48 (2005) 949-964
40. Jubran M., and Widenfalk J. Repair of peripheral nerve transections with fibrin sealant containing neurotrophic factors. Experimental Neurology 181 (2003) 204-212
41. Kaplitt M.G., Feigin A., Tang C., Fitzsimons H.L., Mattis P., Lawlor P.A., et al. Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson's disease: An open label, phase I trial. Lancet 369 (2007) 2097-2105
42. Kaplitt M.G., Leone P., Samulski R.J., Xiao X., Pfaff D.W., O'Malley K.L., et al. Long-term gene expression and phenotypic correction using adeno-associated virus vectors in the mammalian brain. Nature Genetics 8 (1994) 148-154
43. Kaspar B.K., Llado J., Sherkat N., Rothstein J.D., and Gage F.H. Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model. Science 301 (2003) 839-842
44. Kordower J.H., Emborg M.E., Bloch J., Ma S.Y., Chu Y., Leventhal L., et al. Neurodegeneration prevented by lentiviral vector delivery of GDNF in primate models of Parkinson's disease. Science 290 (2000) 767-773
45. Lena A.M., Giannetti P., Sporeno E., Ciliberto G., and Savino R. Immune responses against tetracycline-dependent transactivators affect long-term expression of mouse erythropoietin delivered by a helper-dependent adenoviral vector. Journal of Gene Medicine 7 (2005) 1086-1096
46. Lundborg G. A 25-year perspective of peripheral nerve surgery: Evolving neuroscientific concepts and clinical significance. Journal of Hand Surgery [American Version] 25 (2000) 391-414
47. MacKinnon S.E., and Dellon A.L. Surgery of the peripheral nerve (1988), Thieme Medical Publishers, Inc, New York
48. Madison R.D., Archibald S.J., Lacin R., and Krarup C. Factors contributing to preferential motor reinnervation in the primate peripheral nervous system. Journal of Neuroscience 19 (1999) 11007-11016
49. Maggi S.P., Lowe III J.B., and Mackinnon S.E. Pathophysiology of nerve injury. Clinical Plastic Surgery 30 (2003) 109-126
50. Malessy M.J., and Pondaag W. Obstetric brachial plexus injuries. Neurosurgery Clinics of North America 20 (2009) 1-14 v.
51. Malessy M.J., Thomeer R.T., and van Dijk J.G. Changing central nervous system control following intercostal nerve transfer. Journal of Neurosurgery 89 (1998) 568-574
52. Malessy M.J., van der Kamp W., Thomeer R.T., and van Dijk J.G. Cortical excitability of the biceps muscle after intercostal-to-musculocutaneous nerve transfer. Neurosurgery 42 (1998) 787-794 Discussion pp. 794-785.
53. Martini R., Schachner M., and Brushart T.M. The L2/HNK-1 carbohydrate is preferentially expressed by previously motor axon-associated Schwann cells in reinnervated peripheral nerves. Journal of Neuroscience 14 (1994) 7180-7191
54. Moradzadeh A., Borschel G.H., Luciano J.P., Whitlock E.L., Hayashi A., Hunter D.A., et al. The impact of motor and sensory nerve architecture on nerve regeneration. Experimental Neurology 212 (2008) 370-376
55. Morgenstern D.A., Asher R.A., Naidu M., Carlstedt T., Levine J.M., and Fawcett J.W. Expression and glycanation of the NG2 proteoglycan in developing, adult, and damaged peripheral nerve. Molecular and Cellular Neuroscience 24 (2003) 787-802
56. Nguyen Q.T., Sanes J.R., and Lichtman J.W. Pre-existing pathways promote precise projection patterns. Natural Neuroscience 5 (2002) 861-867
57. Pezet S., and McMahon S.B. Neurotrophins: Mediators and modulators of pain. Annual Review of Neuroscience 29 (2006) 507-538
58. Pondaag W., and Malessy M.J. Recovery of hand function following nerve grafting and transfer in obstetric brachial plexus lesions. Journal of Neurosurgery 105 (2006) 33-40
59. Ramos L.E., and Zell J.P. Rehabilitation program for children with brachial plexus and peripheral nerve injury. Seminars of Pediatric Neurology 7 (2000) 52-57
60. Redett R., Jari R., Crawford T., Chen Y.G., Rohde C., and Brushart T.M. Peripheral pathways regulate motoneuron collateral dynamics. Journal of Neuroscience 25 (2005) 9406-9412
61. Reza J.N., Gavazzi I., and Cohen J. Neuropilin-1 is expressed on adult mammalian dorsal root ganglion neurons and mediates semaphorin3a/collapsin-1-induced growth cone collapse by small diameter sensory afferents. Molecular Cellular Neuroscience 14 (1999) 317-326
62. Skorpil M., Engstrom M., and Nordell A. Diffusion-direction-dependent imaging: A novel MRI approach for peripheral nerve imaging. Magnetic Resonance Imaging 25 (2007) 406-411
63. Stokols S., Sakamoto J., Breckon C., Holt T., Weiss J., and Tuszynski M.H. Templated agarose scaffolds support linear axonal regeneration. Tissue Engineering 12 (2006) 2777-2787
64. Stokols S., and Tuszynski M.H. The fabrication and characterization of linearly oriented nerve guidance scaffolds for spinal cord injury. Biomaterials 25 (2004) 5839-5846
65. Streppel M., Azzolin N., Dohm S., Guntinas-Lichius O., Haas C., Grothe C., et al. Focal application of neutralizing antibodies to soluble neurotrophic factors reduces collateral axonal branching after peripheral nerve lesion. European Journal of Neuroscience 15 (2002) 1327-1342
66. Sunderland S. Nerve injuries and their repair: A critical appraisal (1991), Chuchill Livingstone, Melbourne
67. Tannemaat M.R., Boer G.J., Verhaagen J., and Malessy M.J. Genetic modification of human sural nerve segments by a lentiviral vector encoding nerve growth factor. Neurosurgery 61 (2007) 1286-1294 Discussion pp. 1294-1286.
68. Tannemaat M.R., Eggers R., Hendriks W.T., de Ruiter G.C., van Heerikhuize J.J., Pool C.W., et al. Differential effects of lentiviral vector-mediated overexpression of nerve growth factor and glial cell line-derived neurotrophic factor on regenerating sensory and motor axons in the transected peripheral nerve. European of Journal Neuroscience 28 (2008) 1467-1479
69. Tannemaat M.R., Korecka J., Ehlert E.M., Mason M.R., van Duinen S.G., Boer G.J., et al. Human neuroma contains increased levels of semaphorin 3A, which surrounds nerve fibers and reduces neurite extension in vitro. Journal of Neuroscience 27 (2007) 14260-14264
70. Tannemaat M.R., Verhaagen J., and Malessy M. The application of viral vectors to enhance regeneration after peripheral nerve repair. Neurological Research 30 (2008) 1039-1046
71. Tuszynski M.H., Thal L., Pay M., Salmon D.P., U H.S., Bakay R., et al. A phase 1 clinical trial of nerve growth factor gene therapy for Alzheimer disease. Nature Medicine 11 (2005) 551-555
72. Tzarfati-Majar V., Burstyn-Cohen T., and Klar A. F-spondin is a contact-repellent molecule for embryonic motor neurons. Proceedings of National Academy Science USA 98 (2001) 4722-4727
73. Van den Borne S.W., Isobe S., Verjans J., Petrov A., Lovhaug D., Li P., et al. Molecular imaging of post-infarction cardiac remodeling and effects of anti-angiotensin in therapy. Circulation 116 (2007) 289-290
74. van Dijk J.G., Pondaag W., and Malessy M.J. Botulinum toxin and the pathophysiology of obstetric brachial plexus lesions. Developmental Medicine and Child Neurology 49 (2007) 318 Author reply pp. 318-319.
75. Vergara C., and Ramirez B. CNTF, a pleiotropic cytokine: Emphasis on its myotrophic role. Brain Research and Brain Research Reviews 47 (2004) 161-173
76. Waters P.M. Comparison of the natural history, the outcome of microsurgical repair, and the outcome of operative reconstruction in brachial plexus birth palsy. Journal of Bone Joint Surgery America 81 (1999) 649-659
77. Werner S.R., Mescher A.L., Neff A.W., King M.W., Chaturvedi S., Duffin K.L., et al. Neural MMP-28 expression precedes myelination during development and peripheral nerve repair. Developmental Dynamics 236 (2007) 2852-2864
78. Yanez-Munoz R.J., Balaggan K.S., MacNeil A., Howe S.J., Schmidt M., Smith A.J., et al. Effective gene therapy with nonintegrating lentiviral vectors. Nature Medicine 12 (2006) 348-353
79. Yin Q., Kemp G.J., Yu L.G., Wagstaff S.C., and Frostick S.P. Neurotrophin-4 delivered by fibrin glue promotes peripheral nerve regeneration. Muscle Nerve 24 (2001) 345-351
80. Young C., Miller. E., Nicklous D.M., and Hoffman J.R. Nerve growth factor and neurotrophin-3 affect functional recovery following peripheral nerve injury differently. Restorative Neurology and Neuroscience 18 (2001) 167-175