Lentiviral Vector-Mediated Gradients of GDNF in the Injured Peripheral Nerve: Effects on Nerve Coil Formation, Schwann Cell Maturation and Myelination

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Eggers, Ruben ^a   de Winter, Fred ^a,b   Hoyng, Stefan A ^a,b   Roet, Kasper C D ^a   Ehlert, Erich M ^a   Malessy, Martijn J A ^a,b   Verhaagen, Joost ^a,c   Tannemaat, Martijn R ^a,b  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINE ACETYLTRANSFERASE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GREEN FLUORESCENT PROTEIN; LENTIVIRUS VECTOR; MYELIN BASIC PROTEIN; PROTEIN P75; PROTEIN S 100;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DENSITY; CELL MATURATION; CELL PROLIFERATION; CELL REGENERATION; CELL STRUCTURE; CELL SURVIVAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG DOSE COMPARISON; FEMALE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; MOTONEURON; MYELINATION; NERVE FIBER; NERVE SPROUTING; NONHUMAN; RAT; SCHWANN CELL; SCIATIC NERVE; SCIATIC NERVE INJURY; TREATMENT OUTCOME; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; AXONS; CELL SURVIVAL; FEMALE; GENE EXPRESSION; GENETIC VECTORS; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; LENTIVIRUS; MOTOR NEURONS; MYELIN SHEATH; NERVE REGENERATION; PERIPHERAL NERVE INJURIES; RATS; SCHWANN CELLS; SCIATIC NERVE; TIME FACTORS; TRANSDUCTION, GENETIC;

EID: 84881483389     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071076     Document Type: Article

References (37)

1. Höke A, (2006) Mechanisms of Disease: what factors limit the success of peripheral nerve regeneration in humans? Nat Clin Pract Neurol 2: 448-454 doi:10.1038/ncpneuro0262.
2. Gilbert A, Pivato G, Kheiralla T, (2006) Long-term results of primary repair of brachial plexus lesions in children. Microsurgery 26: 334-342 doi:10.1002/micr.20248.
3. Eggers R, Tannemaat MR, Ehlert EM, Verhaagen J, (2010) A spatio-temporal analysis of motoneuron survival, axonal regeneration and neurotrophic factor expression after lumbar ventral root avulsion and implantation. Exp Neurol 223: 207-220 doi:10.1016/j.expneurol.2009.07.021.
4. Wu W, Han K, Li L, Schinco FP, (1994) Implantation of PNS graft inhibits the induction of neuronal nitric oxide synthase and enhances the survival of spinal motoneurons following root avulsion. Exp Neurol 129: 335-339 doi:10.1006/exnr.1994.1176.
5. Hoang TX, Nieto JH, Dobkin BH, Tillakaratne NJK, Havton LA, (2006) Acute implantation of an avulsed lumbosacral ventral root into the rat conus medullaris promotes neuroprotection and graft reinnervation by autonomic and motor neurons. Neuroscience 138: 1149-1160 doi:10.1016/j.neuroscience.2005.11.066.
6. Höke A, Gordon T, Zochodne DW, Sulaiman OAR, (2002) A decline in glial cell-line-derived neurotrophic factor expression is associated with impaired regeneration after long-term Schwann cell denervation. Exp Neurol 173: 77-85 doi:10.1006/exnr.2001.7826.
7. Mason MRJ, Tannemaat MR, Malessy MJA, Verhaagen J, (2011) Gene therapy for the peripheral nervous system: a strategy to repair the injured nerve? Curr Gene Ther 11: 75-89.
8. Li L, Wu W, Lin LF, Lei M, Oppenheim RW, et al. (1995) Rescue of adult mouse motoneurons from injury-induced cell death by glial cell line-derived neurotrophic factor. Proc Natl Acad Sci USA 92: 9771-9775.
9. Henderson CE, Phillips HS, Pollock RA, Davies AM, Lemeulle C, et al. (1994) GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science 266: 1062-1064.
10. Eggers R, Hendriks WTJ, Tannemaat MR, van Heerikhuize JJ, Pool CW, et al. (2008) Neuroregenerative effects of lentiviral vector-mediated GDNF expression in reimplanted ventral roots. Mol Cell Neurosci 39: 105-117 doi:10.1016/j.mcn.2008.05.018.
11. Tannemaat MR, Eggers R, Hendriks WT, de Ruiter GCW, van Heerikhuize JJ, et al. (2008) 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. Eur J Neurosci 28: 1467-1479 doi:10.1111/j.1460-9568.2008.06452.x.
12. Santosa KB, Jesuraj NJ, Viader A, MacEwan M, Newton P, et al. (2013) Nerve allografts supplemented with schwann cells overexpressing glial-cell-line-derived neurotrophic factor. Muscle Nerve 47: 213-223 doi:10.1002/mus.23490.
13. Blits B, Carlstedt TP, Ruitenberg MJ, de Winter F, Hermens WTJMC, et al. (2004) 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. Exp Neurol 189: 303-316 doi:10.1016/j.expneurol.2004.05.014.
14. Chu T-H, Li S-Y, Guo A, Wong W-M, Yuan Q, et al. (2009) Implantation of neurotrophic factor-treated sensory nerve graft enhances survival and axonal regeneration of motoneurons after spinal root avulsion. J Neuropathol Exp Neurol 68: 94-101 doi:10.1097/NEN.0b013e31819344a9.
15. Mai L, Jope RS, Li X, (2002) BDNF-mediated signal transduction is modulated by GSK3beta and mood stabilizing agents. J Neurochem 82: 75-83.
16. Batchelor PE, Porritt MJ, Martinello P, Parish CL, Liberatore GT, et al. (2002) Macrophages and Microglia Produce Local Trophic Gradients That Stimulate Axonal Sprouting Toward but Not beyond the Wound Edge. Mol Cell Neurosci 21: 436-453.
17. Lin Y-C, Ramadan M, Hronik-Tupaj M, Kaplan DL, Philips BJ, et al. (2011) Spatially controlled delivery of neurotrophic factors in silk fibroin-based nerve conduits for peripheral nerve repair. Ann Plast Surg 67: 147-155 doi:10.1097/SAP.0b013e3182240346.
18. Bonner JF, Blesch A, Neuhuber B, Fischer I, (2010) Promoting directional axon growth from neural progenitors grafted into the injured spinal cord. J Neurosci Res 88: 1182-1192 doi:10.1002/jnr.22288.
19. Taylor L, Jones L, Tuszynski MH, Blesch A, (2006) Neurotrophin-3 gradients established by lentiviral gene delivery promote short-distance axonal bridging beyond cellular grafts in the injured spinal cord. J Neurosci 26: 9713-9721 doi:10.1523/JNEUROSCI.0734-06.2006.
20. Magill CK, Moore AM, Yan Y, Tong AY, MacEwan MR, et al. (2010) The differential effects of pathway- versus target-derived glial cell line-derived neurotrophic factor on peripheral nerve regeneration. J Neurosurg 113: 102-109 doi:10.3171/2009.10.JNS091092.
21. Hase A, Saito F, Yamada H, Arai K, Shimizu T, et al. (2005) Characterization of glial cell line-derived neurotrophic factor family receptor alpha-1 in peripheral nerve Schwann cells. J Neurochem 95: 537-543 doi:10.1111/j.1471-4159.2005.03391.x.
22. Höke A, Ho T, Crawford TO, LeBel C, Hilt D, et al. (2003) Glial cell line-derived neurotrophic factor alters axon schwann cell units and promotes myelination in unmyelinated nerve fibers. J Neurosci 23: 561-567.
23. Hendriks WTJ, Eggers R, Carlstedt TP, Zaldumbide A, Tannemaat MR, et al. (2007) Lentiviral vector-mediated reporter gene expression in avulsed spinal ventral root is short-term, but is prolonged using an immune "stealth" transgene. Restor Neurol Neurosci 25: 585-599.
24. Ossevoort M, Visser BMJ, van den Wollenberg DJM, van der Voort EIH, Offringa R, et al. (2003) Creation of immune "stealth" genes for gene therapy through fusion with the Gly-Ala repeat of EBNA-1. Gene Ther 10: 2020-2028 doi:10.1038/sj.gt.3302098.
25. Jessen KR, Mirsky R, (2002) Signals that determine Schwann cell identity. J Anat 200: 367-376.
26. Salvatore MF, Ai Y, Fischer B, Zhang AM, Grondin RC, et al. (2006) Point source concentration of GDNF may explain failure of phase II clinical trial. Exp Neurol 202: 497-505 doi:10.1016/j.expneurol.2006.07.015.
27. Ai Y, Markesbery W, Zhang Z, Grondin R, Elseberry D, et al. (2003) Intraputamenal infusion of GDNF in aged rhesus monkeys: distribution and dopaminergic effects. J Comp Neurol 461: 250-261 doi:10.1002/cne.10689.
28. Iwase T, Jung CG, Bae H, Zhang M, Soliven B, (2005) Glial cell line-derived neurotrophic factor-induced signaling in Schwann cells. J Neurochem 94: 1488-1499 doi:10.1111/j.1471-4159.2005.03290.x.
29. Zhang L, Ma Z, Smith GM, Wen X, Pressman Y, et al. (2009) GDNF-enhanced axonal regeneration and myelination following spinal cord injury is mediated by primary effects on neurons. Glia 57: 1178-1191 doi:10.1002/glia.20840.
30. Heermann S, Spittau B, Zajzon K, Schwab MH, Krieglstein K, (2012) Schwann cells migrate along axons in the absence of GDNF signaling. BMC Neurosci 13: 92 doi:10.1186/1471-2202-13-92.
31. Mirsky R, Woodhoo A, Parkinson DB, Arthur-Farraj P, Bhaskaran A, et al. (2008) Novel signals controlling embryonic Schwann cell development, myelination and dedifferentiation. J Peripher Nerv Syst 13: 122-135 doi:10.1111/j.1529-8027.2008.00168.x.
32. Batchelor PE, Liberatore GT, Porritt MJ, Donnan GA, Howells DW, (2000) Inhibition of brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor expression reduces dopaminergic sprouting in the injured striatum. Eur J Neurosci 12: 3462-3468.
33. Georgievska B, Kirik D, Björklund A, (2002) Aberrant sprouting and downregulation of tyrosine hydroxylase in lesioned nigrostriatal dopamine neurons induced by long-lasting overexpression of glial cell line derived neurotrophic factor in the striatum by lentiviral gene transfer. Exp Neurol 177: 461-474.
34. Nguyen QT, Parsadanian AS, Snider WD, Lichtman JW, (1998) Hyperinnervation of neuromuscular junctions caused by GDNF overexpression in muscle. Science 279: 1725-1729.
35. Zwick M, Teng L, Mu X, Springer JE, Davis BM, (2001) Overexpression of GDNF induces and maintains hyperinnervation of muscle fibers and multiple end-plate formation. Exp Neurol 171: 342-350 doi:10.1006/exnr.2001.7753.
36. Keller-Peck CR, Feng G, Sanes JR, Yan Q, Lichtman JW, et al. (2001) Glial cell line-derived neurotrophic factor administration in postnatal life results in motor unit enlargement and continuous synaptic remodeling at the neuromuscular junction. J Neurosci 21: 6136-6146.
37. Zaldumbide A, Weening S, Cramer SJ, Rabelink MJWE, Verhaagen J, et al. (2010) A potentially immunologically inert derivative of the reverse tetracycline-controlled transactivator. Biotechnol Lett 32: 749-754 doi:10.1007/s10529-010-0218-8.