Gene therapy approaches to enhance regeneration of the injured peripheral nerve

European Journal of Pharmacology

Volumn 719, Issue 1-3, 2013, Pages 145-152

  De Winter, Fred ^a   Hoyng, Stefan ^a,b   Tannemaat, Martijn ^a,b   Eggers, Ruben ^a   Mason, Matthew ^a   Malessy, Martijn ^a,b   Verhaagen, Joost ^a,c  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

Adeno associated viral vector; Gene therapy; Lentiviral vector; Peripheral nerve

Indexed keywords

PARVOVIRUS VECTOR; TRANSCRIPTION FACTOR;

BIOTECHNOLOGY; CELL ADHESION; DISEASE MODEL; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENE TARGETING; GENE THERAPY; HUMAN; IMMUNE RESPONSE; MOTONEURON; NERVE CELL; NERVE REGENERATION; NONHUMAN; PERIPHERAL NERVE; PERIPHERAL NERVE INJURY; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; REVIEW; RODENT; SCHWANN CELL; SPINAL GANGLION; VIRUS GENE;

ADENO-ASSOCIATED VIRAL VECTOR; GENE THERAPY; LENTIVIRAL VECTOR; PERIPHERAL NERVE;

ANIMALS; DEPENDOVIRUS; GENETIC THERAPY; HUMANS; NERVE REGENERATION; NEURONS; PERIPHERAL NERVE INJURIES; SCHWANN CELLS;

EID: 84888294625     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2013.04.057     Document Type: Review

References (94)

1. M.R. Andrews, S. Czvitkovich, E. Dassie, C.F. Vogelaar, A. Faissner, B. Blits, F.H. Gage, C. ffrench-Constant, and J.W. Fawcett Alpha9 integrin promotes neurite outgrowth on tenascin-C and enhances sensory axon regeneration Journal of Neruroscience 29 2009 5546 5557
2. P.J. Arthur-Farraj, M. Latouche, D.K. Wilton, S. Quintes, E. Chabrol, A. Banerjee, A. Woodhoo, B. Jenkins, M. Rahman, M. Turmaine, G.K. Wicher, R. Mitter, L. Greensmith, A. Behrens, G. Raivich, R. Mirsky, and K.R. Jessen c-Jun reprograms Schwann cells of injured nerves to generate a repair cell essential for regeneration Neuron 75 2012 633 647
3. F.M. Bareyre, N. Garzorz, C. Lang, T. Misgeld, H. Buning, and M. Kerschensteiner In vivo imaging reveals a phase-specific role of STAT3 during central and peripheral nervous system axon regeneration Proceedings of the National Academy of Sciences USA 108 2011 6282 6287
4. L.I. Benowitz, V.E. Shashoua, and M.G. Yoon Specific changes in rapidly transported proteins dur (Pubitemid 11011799)
5. B. Blits, T.P. Carlstedt, M.J. Ruitenberg, W.F. de, W.T. Hermens, P.A. Dijkhuizen, J.W. Claasens, R. Eggers, R. van der Sluis, L. Tenenbaum, G.J. Boer, and J. Verhaagen 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 (Pubitemid 39221824)
6. N.M. Boulis, A.J. Noordmans, D.K. Song, M.J. Imperiale, A. Rubin, P. Leone, M. During, and E.L. Feldman Adeno-associated viral vector gene expression in the adult rat spinal cord following remote vector delivery Neurobiology of Disease 14 2003 535 541 (Pubitemid 37543531)
7. T.M. Brushart Nerve Repair 2011 Oxford University Press
8. A. Buffo, A.J. Holtmaat, T. Savio, J.S. Verbeek, J. Oberdick, A.B. Oestreicher, W.H. Gispen, J. Verhaagen, F. Rossi, and P. Strata Targeted overexpression of the neurite growth-associated protein B-50/GAP-43 in cerebellar Purkinje cells induces sprouting after axotomy but not axon regeneration into growth-permissive transplants Journal of Neruroscience 17 1997 8778 8791 (Pubitemid 27481744)
9. T.H. Chu, S.Y. Li, A. Guo, W.M. Wong, Q. Yuan, and W. Wu Implantation of neurotrophic factor-treated sensory nerve graft enhances survival and axonal regeneration of motoneurons after spinal root avulsion Journal of Neruropathy and Experimental Nerurology 68 2009 94 101
10. J. De Wit, R. Eggers, R. Evers, E. Castren, and J. Verhaagen Long-term adeno-associated viral vector-mediated expression of truncated TrkB in the adult rat facial nucleus results in motor neuron degeneration Journal of Neruroscience 26 2006 1516 1530 (Pubitemid 43237022)
11. P.A. Dijkhuizen, R.J. Pasterkamp, W.T. Hermens, W.F. de, R.J. Giger, and J. Verhaagen Adenoviral vector-mediated gene delivery to injured rat peripheral nerve Journal of Neurotrauma 15 1998 387 397 (Pubitemid 28262273)
12. A.T. Dobson, F. Sederati, G. vi-Rao, W.M. Flanagan, M.J. Farrell, J.G. Stevens, E.K. Wagner, and L.T. Feldman Identification of the latency-associated transcript promoter by expression of rabbit beta-globin mRNA in mouse sensory nerve ganglia latently infected with a recombinant herpes simplex virus Journal of Virology 63 1989 3844 3851 (Pubitemid 19205457)
13. P.M. Edwards, C.E. Van der Zee, J. Verhaagen, P. Schotman, F.G. Jennekens, and W.H. Gispen Evidence that the neurotrophic actions of alpha-MSH may derive from its ability to mimick the actions of a peptide formed in degenerating nerve stumps Journal of the Neurological Sciences 64 1984 333 340 (Pubitemid 14118947)
14. R. Eggers, W.T. Hendriks, M.R. Tannemaat, J.J. van Heerikhuize, C.W. Pool, T.P. Carlstedt, A. Zaldumbide, R.C. Hoeben, G.J. Boer, and J. Verhaagen Neuroregenerative effects of lentiviral vector-mediated GDNF expression in reimplanted ventral roots Molecular and Cellular Neuroscience 39 2008 105 117
15. R. Eggers, M.R. Tannemaat, E.M. Ehlert, and J. Verhaagen A spatio-temporal analysis of motoneuron survival, axonal regeneration and neurotrophic factor expression after lumbar ventral root avulsion and implantation Experimental Neurology 223 2010 207 220
16. J. Fleming, S.L. Ginn, R.P. Weinberger, T.N. Trahair, J.A. Smythe, and I.E. Alexander Adeno-associated virus and lentivirus vectors mediate efficient and sustained transduction of cultured mouse and human dorsal root ganglia sensory neurons Human Gene Therapy 12 2001 77 86 (Pubitemid 32044469)
17. H. Funakoshi, J. Frisen, G. Barbany, T. Timmusk, O. Zachrisson, V.M. Verge, and H. Persson Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve Journal of Cell Biology 123 1993 455 465 (Pubitemid 23313968)
18. A.I. Geller, and X.O. Breakefield A defective HSV-1 vector expresses Escherichia coli beta-galactosidase in cultured peripheral neurons Science 241 1988 1667 1669
19. M. Glatzel, E. Flechsig, B. Navarro, M.A. Klein, J.C. Paterna, H. Bueler, and A. Aguzzi Adenoviral and adeno-associated viral transfer of genes to the peripheral nervous system Proceedings of the National Academy of Sciences USA 97 2000 442 447 (Pubitemid 30055850)
20. T. Gordon, N. Amirjani, D.C. Edwards, and K.M. Chan Brief post-surgical electrical stimulation accelerates axon regeneration and muscle reinnervation without affecting the functional measures in carpal tunnel syndrome patients Experimental Neurology 223 2010 192 202
21. T. Gordon, N. Tyreman, and M.A. Raji The basis for diminished functional recovery after delayed peripheral nerve repair Journal of Neuroscience 31 2011 5325 5334
22. J.C. Grieger, V.W. Choi, and R.J. Samulski Production and characterization of adeno-associated viral vectors Nature Protocols 1 2006 1412 1428
23. D. Grimm, A. Kern, K. Rittner, and J.A. Kleinschmidt Novel tools for production and purification of recombinant adenoassociated virus vectors Human Gene Therapy 9 1998 2745 2760 (Pubitemid 29027018)
24. V. Guenard, B. Schweitzer, E. Flechsig, S. Hemmi, R. Martini, U. Suter, and M. Schachner Effective gene transfer of lacZ and P0 into Schwann cells of P0-deficient mice Glia 25 1999 165 178 (Pubitemid 29032772)
25. H. Hammarberg, F. Piehl, S. Cullheim, J. Fjell, T. Hokfelt, and K. Fried GDNF mRNA in Schwann cells and DRG satellite cells after chronic sciatic nerve injury NeuroReport 7 1996 857 860 (Pubitemid 26167964)
26. A. Hase, F. Saito, H. Yamada, K. Arai, T. Shimizu, and K. Matsumura Characterization of glial cell line-derived neurotrophic factor family receptor alpha-1 in peripheral nerve Schwann cells Journal of Neurochemistry 95 2005 537 543 (Pubitemid 41457521)
27. W.T. Hendriks, R. Eggers, T.P. Carlstedt, A. Zaldumbide, M.R. Tannemaat, F.J. Fallaux, R.C. Hoeben, G.J. Boer, and J. Verhaagen 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 (Pubitemid 351525720)
28. W.T. Hermens, B.O. ter, P.A. Dijkhuizen, M.A. Sonnemans, D. Grimm, J.A. Kleinschmidt, and J. Verhaagen Purification of recombinant adeno-associated virus by iodixanol gradient ultracentrifugation allows rapid and reproducible preparation of vector stocks for gene transfer in the nervous system Human Gene Therapy 10 1999 1885 1891 (Pubitemid 29357694)
29. W.T. Hermens, and J. Verhaagen Adenoviral vector-mediated gene expression in the nervous system of immunocompetent Wistar and T cell-deficient nude rats: preferential survival of transduced astroglial cells in nude rats Human Gene Therapy 8 1997 1049 1063 (Pubitemid 27308203)
30. D.Y. Ho, and E.S. Mocarski Beta-galactosidase as a marker in the peripheral and neural tissues of the herpes simplex virus-infected mouse Virology 167 1988 279 283
31. A. Hoke Mechanisms of Disease: what factors limit the success of peripheral nerve regeneration in humans? Nature Clinical Practice Neurology 2 2006 448 454 (Pubitemid 44137946)
32. A. Hoke, C. Cheng, and D.W. Zochodne Expression of glial cell line-derived neurotrophic factor family of growth factors in peripheral nerve injury in rats NeuroReport 11 2000 1651 1654 (Pubitemid 30350327)
33. A. Hoke, T. Ho, T.O. Crawford, C. LeBel, D. Hilt, and J.W. Griffin Glial cell line-derived neurotrophic factor alters axon schwann cell units and promotes myelination in unmyelinated nerve fibers Journal of Neuroscience 23 2003 561 567 (Pubitemid 36139555)
34. A.J. Holtmaat, P.A. Dijkhuizen, A.B. Oestreicher, H.J. Romijn, N.M. Van der Lugt, A. Berns, F.L. Margolis, W.H. Gispen, and J. Verhaagen Directed expression of the growth-associated protein B-50/GAP-43 to olfactory neurons in transgenic mice results in changes in axon morphology and extraglomerular fiber growth Journal of Neuroscience 15 1995 7953 7965 (Pubitemid 26006902)
35. A.J. Holtmaat, W.T. Hermens, M.A. Sonnemans, R.J. Giger, F.W. Van Leeuwen, M.G. Kaplitt, A.B. Oestreicher, W.H. Gispen, and J. Verhaagen Adenoviral vector-mediated expression of B-50/GAP-43 induces alterations in the membrane organization of olfactory axon terminals in vivo Journal of Neuroscience 17 1997 6575 6586 (Pubitemid 27366610)
36. A.J. Holtmaat, A.B. Oestreicher, W.H. Gispen, and J. Verhaagen Manipulation of gene expression in the mammalian nervous system: application in the study of neurite outgrowth and neuroregeneration-related proteins Brain Research: Brain Research Reviews 26 1998 43 71 (Pubitemid 28179009)
37. J. Homs, L. Ariza, G. Pages, E. Udina, X. Navarro, M. Chillon, and A. Bosch Schwann cell targeting via intrasciatic injection of AAV8 as gene therapy strategy for peripheral nerve regeneration Gene Therapy 18 2011 622 630
38. S.A. Hoyng, M.R. Tannemaat, W.F. de, J. Verhaagen, and M.J. Malessy Nerve surgery and gene therapy: a neurobiological and clinical perspective Journal of Hand Surgery (European Volume) 36 2011 735 746
39. Y. Hu, S.G. Leaver, G.W. Plant, W.T. Hendriks, S.P. Niclou, J. Verhaagen, A.R. Harvey, and Q. Cui Lentiviral-mediated transfer of CNTF to schwann cells within reconstructed peripheral nerve grafts enhances adult retinal ganglion cell survival and axonal regeneration Molecular Therapy 11 2005 906 915 (Pubitemid 40724109)
40. M.G. Kaplitt, A. Feigin, C. Tang, H.L. Fitzsimons, P. Mattis, P.A. Lawlor, R.J. Bland, D. Young, K. Strybing, D. Eidelberg, and M.J. During 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 (Pubitemid 46935946)
41. M.G. Kaplitt, P. Leone, R.J. Samulski, X. Xiao, D.W. Pfaff, K.L. O'Malley, and M.J. During Long-term gene expression and phenotypic correction using adeno-associated virus vectors in the mammalian brain Nature Genetics 8 1994 148 154 (Pubitemid 24308362)
42. B.K. Kaspar, J. Llado, N. Sherkat, J.D. Rothstein, and F.H. Gage Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model Science 301 2003 839 842 (Pubitemid 36962626)
43. R.H. Kutner, X.Y. Zhang, and J. Reiser Production, concentration and titration of pseudotyped HIV-1-based lentiviral vectors Nature Protocol 4 2009 495 505
44. B. Lorber, M.L. Howe, L.I. Benowitz, and N. Irwin Mst3b, an Ste20-like kinase, regulates axon regeneration in mature CNS and PNS pathways Nature Neuroscience 12 2009 1407 1414
45. H.D. Macgillavry, J. Cornelis, L.R. van der Kallen, M.M. Sassen, J. Verhaagen, A.B. Smit, and R.E. van Kesteren Genome-wide gene expression and promoter binding analysis identifies NFIL3 as a repressor of C/EBP target genes in neuronal outgrowth Molecular and Cellular Neuroscience 46 2011 460 468
46. H.D. Macgillavry, F.J. Stam, M.M. Sassen, L. Kegel, W.T. Hendriks, J. Verhaagen, A.B. Smit, and R.E. van Kesteren NFIL3 and cAMP response element-binding protein form a transcriptional feedforward loop that controls neuronal regeneration-associated gene expression Journal of Neuroscience 29 2009 15542 15550
47. M. Makwana, and G. Raivich Molecular mechanisms in successful peripheral regeneration FEBS Journal 272 2005 2628 2638 (Pubitemid 40825411)
48. M.J. Malessy, and W. Pondaag Obstetric brachial plexus injuries Neurosurgery Clinics of North America 20 2009 1 14
49. M.R. Mason, E.M. Ehlert, R. Eggers, C.W. Pool, S. Hermening, A. Huseinovic, E. Timmermans, B. Blits, and J. Verhaagen Comparison of AAV serotypes for gene delivery to dorsal root ganglion neurons Molecular Therapy 18 2010 715 724
50. M.R. Mason, M.R. Tannemaat, M.J. Malessy, and J. Verhaagen Gene therapy for the peripheral nervous system: a strategy to repair the injured nerve? Current Gene Therapy 11 2011 75 89
51. T.J. McCown, X. Xiao, J. Li, G.R. Breese, and R.J. Samulski Differential and persistent expression patterns of CNS gene transfer by an adeno-associated virus (AAV) vector Brain Research 713 1996 99 107 (Pubitemid 26114833)
52. D.L. Moore, M.G. Blackmore, Y. Hu, K.H. Kaestner, J.L. Bixby, V.P. Lemmon, and J.L. Goldberg KLF family members regulate intrinsic axon regeneration ability Science 326 2009 298 301
53. P. Naveilhan, W.M. ElShamy, and P. Ernfors Differential regulation of mRNAs for GDNF and its receptors Ret and GDNFR alpha after sciatic nerve lesion in the mouse European Journal of Neuroscience 9 1997 1450 1460 (Pubitemid 27303245)
54. S. Nayak, and R.W. Herzog Progress and prospects: immune responses to viral vectors Gene Therapy 17 2010 295 304
55. A.B. Oestreicher, P.N. de Graan, W.H. Gispen, J. Verhaagen, and L.H. Schrama B-50, the growth associated protein-43: modulation of cell morphology and communication in the nervous system Progress in Neurobiology 53 1997 627 686 (Pubitemid 28023417)
56. A.B. Oestreicher, H. Zwiers, P. Schotman, and W.H. Gispen Immunohistochemical localization of a phosphoprotein (B-50) isolated from rat brain synaptosomal plasma membranes Brain Research Bulletin 6 1981 145 153 (Pubitemid 11102120)
57. P.P.A. Oranje, P. Verheesen, D. Verbart, Y. Mijnsbergen, H.J.W. Haard, P. Hermans, M.R. ten Haaft, J. Twisk, P.A. Dijkhuizen, W.T. Hermens, and J.J.M. Meulenberg Isolation of an Adeno-Associated Virus (AAV)-Specific Camelid-Derived Single Chain Antibody Fragment: A Novel Tool for Purification of AAV Vectors of Different Serotypes Molecular Therapy 9 S1 2004 S162
58. P. Parikh, Y. Hao, M. Hosseinkhani, S.B. Patil, G.W. Huntley, M. Tessier-Lavigne, and H. Zou Regeneration of axons in injured spinal cord by activation of bone morphogenetic protein/Smad1 signaling pathway in adult neurons Proceedings of the National Academy of Sciences USA 108 2011 E99 107
59. A.L. Peel, S. Zolotukhin, G.W. Schrimsher, N. Muzyczka, and P.J. Reier Efficient transduction of green fluorescent protein in spinal cord neurons using adeno-associated virus vectors containing cell type-specific promoters Gene Therapy 4 1997 16 24 (Pubitemid 27073218)
60. M. Pirozzi, A. Quattrini, G. Andolfi, G. Dina, M.C. Malaguti, A. Auricchio, and E.I. Rugarli Intramuscular viral delivery of paraplegin rescues peripheral axonopathy in a model of hereditary spastic paraplegia Journal of Clinical Investigation 116 2006 202 208 (Pubitemid 43121805)
61. G. Raivich, M. Bohatschek, C.C. Da, O. Iwata, M. Galiano, M. Hristova, A.S. Nateri, M. Makwana, L. Riera-Sans, D.P. Wolfer, H.P. Lipp, A. Aguzzi, E.F. Wagner, and A. Behrens The AP-1 transcription factor c-Jun is required for efficient axonal regeneration Neuron. 43 2004 57 67 (Pubitemid 38952819)
62. A. Ries, J.L. Goldberg, and B. Grimpe A novel biological function for CD44 in axon growth of retinal ganglion cells identified by a bioinformatics approach Journal of Neurochemistry 103 2007 1491 1505 (Pubitemid 47631812)
63. F. Rossi, S. Gianola, and L. Corvetti Regulation of intrinsic neuronal properties for axon growth and regeneration Progress in Neurobiology 81 2007 1 28 (Pubitemid 46282271)
64. M.J. Ruitenberg, B. Blits, P.A. Dijkhuizen, E.T. te Beek, A. Bakker, J.J. van Heerikhuize, C.W. Pool, W.T. Hermens, G.J. Boer, and J. Verhaagen Adeno-associated viral vector-mediated gene transfer of brain-derived neurotrophic factor reverses atrophy of rubrospinal neurons following both acute and chronic spinal cord injury Neurobiology of Disease 15 2004 394 406 (Pubitemid 38304891)
65. K.B. Santosa, N.J. Jesuraj, A. Viader, M. Macewan, P. Newton, D.A. Hunter, S.E. Mackinnon, and P.J. Johnson Nerve allografts supplemented with schwann cells overexpressing glial-cell-line-derived neurotrophic factor Muscle and Nerve 47 2013 213 223
66. M.E. Shy, M. Tani, Y.J. Shi, S.A. Whyatt, T. Chbihi, S.S. Scherer, and J. Kamholz An adenoviral vector can transfer lacZ expression into Schwann cells in culture and in sciatic nerve Annals of Neurology 38 1995 429 436
67. J.H. Skene, and M. Willard Changes in axonally transported proteins during axon regeneration in toad retinal ganglion cells Journal of Cell Biology 89 1981 86 95 (Pubitemid 11066133)
68. P.D. Smith, F. Sun, K.K. Park, B. Cai, C. Wang, K. Kuwako, I. Martinez-Carrasco, L. Connolly, and Z. He SOCS3 deletion promotes optic nerve regeneration in vivo Neuron 64 2009 617 623
69. B.R. Snyder, N.M. Boulis, and T. Federici Viral vector-mediated gene transfer for CNS disease Expert Opinion on Biological Therapy 10 2010 381 394
70. B. Storek, M. Reinhardt, C. Wang, W.G. Janssen, N.M. Harder, M.S. Banck, J.H. Morrison, and A.S. Beutler Sensory neuron targeting by self-complementary AAV8 via lumbar puncture for chronic pain Proceedings of the National Academy of Sciences USA 105 2008 1055 1060 (Pubitemid 351282080)
71. F. Sun, K.K. Park, S. Belin, D. Wang, T. Lu, G. Chen, K. Zhang, C. Yeung, G. Feng, B.A. Yankner, and Z. He Sustained axon regeneration induced by co-deletion of PTEN and SOCS3 Nature 480 2011 372 375
72. C.L. Tan, M.R. Andrews, J.C. Kwok, T.G. Heintz, L.F. Gumy, R. Fassler, and J.W. Fawcett Kindlin-1 enhances axon growth on inhibitory chondroitin sulfate proteoglycans and promotes sensory axon regeneration Journal of Neuroscience 32 2012 7325 7335
73. M.R. Tannemaat, R. Eggers, W.T. Hendriks, G.C. de Ruiter, J.J. van Heerikhuize, C.W. Pool, M.J. Malessy, G.J. Boer, and J. Verhaagen 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 Journal of Neuroscience 28 2008 1467 1479
74. G. Tiscornia, O. Singer, and I.M. Verma Production and purification of lentiviral vectors Nature Protocols 1 2006 241 245
75. C. Towne, M. Pertin, A.T. Beggah, P. Aebischer, and I. Decosterd Recombinant adeno-associated virus serotype 6 (rAAV2/6)-mediated gene transfer to nociceptive neurons through different routes of delivery Molecular Pain 5 2009 52
76. C.E. Van der Zee, H.B. Nielander, J.P. Vos, S.S. Lopes da, J. Verhaagen, A.B. Oestreicher, L.H. Schrama, P. Schotman, and W.H. Gispen Expression of growth-associated protein B-50 (GAP43) in dorsal root ganglia and sciatic nerve during regenerative sprouting Journal of Neuroscience 9 1989 3505 3512 (Pubitemid 19260022)
77. C.O. van Hooff, J.C. Holthuis, A.B. Oestreicher, J. Boonstra, P.N. de Graan, and W.H. Gispen Nerve growth factor-induced changes in the intracellular localization of the protein kinase C substrate B-50 in pheochromocytoma PC12 cells Journal of Cell Biology 108 1989 1115 1125 (Pubitemid 19083755)
78. R.E. van Kesteren, M.R. Mason, H.D. Macgillavry, A.B. Smit, and J. Verhaagen A gene network perspective on axonal regeneration Frontiers in Molecular Neuroscience 4 2011 46
79. J. Verhaagen, P.M. Edwards, and W.H. Gispen Damaged rat peripheral nerves do not contain detectable amounts of alpha-MSH Journal of Neuroscience Research 19 1988 14 18 (Pubitemid 18040542)
80. J. Verhaagen, P.M. Edwards, F.G. Jennekens, and W.H. Gispen Pharmacological aspects of the influence of melanocortins on the formation of regenerative peripheral nerve sprouts Peptides 8 1987 581 584 (Pubitemid 17113763)
81. J. Verhaagen, P.M. Edwards, P. Schotman, F.G. Jennekens, and W.H. Gispen Characterization of epitopes shared by alpha-melanocyte-stimulating hormone (alpha-MSH) and the 150-kD neurofilament protein (NF150): relationship to neurotrophic sequences Journal of Neuroscience Research 16 1986 589 600 (Pubitemid 17218439)
82. J. Verhaagen, C.A. Greer, and F.L. Margolis B-50/GAP43 Gene Expression in the Rat Olfactory System During Postnatal Development and Aging European Journal of Neuroscience 2 1990 397 407 (Pubitemid 20170137)
83. J. Verhaagen, W.T. Hermens, P.A. Dijkhuizen, A.J. Holtmaat, and W.H. Gispen Use of viral vectors to promote neuroregeneration Journal of Clinical Neuroscience 3 1995 275 283 (Pubitemid 26372831)
84. J. Verhaagen, W.T. Hermens, M.G. Kaplitt, D.W. Pfaff, and W.H. Gispen B-50/GAP-43 expression via a defective herpes simplex virus vector results in persistent morphological changes in non-neuronal cells Gene Therapy 1 Suppl. 1 1994 S81
85. J. Verhaagen, W.T. Hermens, A.B. Oestreicher, W.H. Gispen, S.D. Rabkin, D.W. Pfaff, and M.G. Kaplitt Expression of the growth-associated protein B-50/GAP43 via a defective herpes-simplex virus vector results in profound morphological changes in non-neuronal cells Brain Research: Molecular Brain Research 26 1994 26 36
86. J. Verhaagen, and J.W. McDonald Spinal cord injury Handbook of Clinical Neurology 109 2012 ix
87. J. Verhaagen, A.B. Oestreicher, W.H. Gispen, and F.L. Margolis The expression of the growth associated protein B50/GAP43 in the olfactory system of neonatal and adult rats Journal of Neuroscience 9 1989 683 691 (Pubitemid 19069512)
88. J. Verhaagen, C.O. van Hooff, P.M. Edwards, P.N. de Graan, A.B. Oestreicher, P. Schotman, F.G. Jennekens, and W.H. Gispen The kinase C substrate protein B-50 and axonal regeneration Brain Research Bulletin 17 1986 737 741 (Pubitemid 17215217)
89. J. Verhaagen, R.E. van Kesteren, K.A. Bossers, H.D. Macgillavry, M.R. Mason, and A.B. Smit Molecular target discovery for neural repair in the functional genomics era Handbook of Clinical Neurology 109 2012 595 616
90. Y. Xu, Y. Gu, P. Wu, G.W. Li, and L.Y. Huang Efficiencies of transgene expression in nociceptive neurons through different routes of delivery of adeno-associated viral vectors Human Gene Therapy 14 2003 897 906 (Pubitemid 36693798)
91. A. Zaldumbide, S. Weening, S.J. Cramer, M.J. Rabelink, J. Verhaagen, and R.C. Hoeben A potentially immunologically inert derivative of the reverse tetracycline-controlled transactivator Biotechnology Letters 32 2010 749 754
92. S. Zolotukhin, B.J. Byrne, E. Mason, I. Zolotukhin, M. Potter, K. Chesnut, C. Summerford, R.J. Samulski, and N. Muzyczka Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield Gene Therapy 6 1999 973 985 (Pubitemid 29295202)
93. S. Zolotukhin, M. Potter, I. Zolotukhin, Y. Sakai, S. Loiler, T.J. Fraites Jr., V.A. Chiodo, T. Phillipsberg, N. Muzyczka, W.W. Hauswirth, T.R. Flotte, B.J. Byrne, and R.O. Snyder Production and purification of serotype 1, 2, and 5 recombinant adeno-associated viral vectors Methods 28 2002 158 167 (Pubitemid 35341079)
94. H. Zwiers, J. Verhaagen, C.J. van Dongen, P.N. de Graan, and W.H. Gispen Resolution of rat brain synaptic phosphoprotein B-50 into multiple forms by two-dimensional electrophoresis: evidence for multisite phosphorylation Journal of Neurochemistry 44 1985 1083 1090 (Pubitemid 15105759)