Immunohistochemical, Ultrastructural and Functional Analysis of Axonal Regeneration through Peripheral Nerve Grafts Containing Schwann Cells Expressing BDNF, CNTF or NT3

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Godinho, Maria João ^a   Teh, Lip ^b   Pollett, Margaret A ^a   Goodman, Douglas ^c   Hodgetts, Stuart I ^a   Sweetman, Iain ^a,e   Walters, Mark ^b   Verhaagen, Joost ^d   Plant, Giles W ^a,f   Harvey, Alan R ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b PRINCESS MARGARET HOSPITAL FOR CHILDREN   (Australia)

^c MURDOCH UNIVERSITY   (Australia)

^d NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^e UNIVERSITY OF OTAGO   (New Zealand)

^f STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA TUBULIN; BETAIII TUBULIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCITONIN GENE RELATED PEPTIDE; CELL ANTIBODY; CILIARY NEUROTROPHIC FACTOR; ISOLECTIN B4; NEUROTROPHIN 3; PANNF ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOGRAFT; CELL COUNT; CELL DENSITY; CELL POPULATION; CELL REGENERATION; CELL SIZE; CELL STRUCTURE; CELL SURVIVAL; CELL TRANSPLANTATION; CONTROLLED STUDY; DNA MODIFICATION; EX VIVO STUDY; GAIT; HINDLIMB; IMMUNOHISTOCHEMISTRY; INTERMETHOD COMPARISON; LOCOMOTION; MALE; MYELINATED NERVE; MYELINATION; NERVE FIBER; NERVE GRAFT; NERVE SHEATH; NONHUMAN; PROTEIN EXPRESSION; RAT; SCHWANN CELL; SENSORY ANALYSIS; SENSORY NERVE CELL; TRANSGENE; ULTRASTRUCTURE; XENOGRAFT;

EID: 84881229413     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069987     Document Type: Article

References (92)

1. Lundborg G, (2000) A 25-year perspective of peripheral nerve surgery: evolving neuroscientific concepts and clinical significance. J Hand Surg 35A: 391-414.
2. Ray WZ, Mackinnon SE, (2010) Management of nerve gaps: autografts, allografts, nerve transfers, and end-to-side neurorrhaphy. Exp Neurol 223: 77-85.
3. Dahlin LB, Brandt J, (2004) Basic science of peripheral nerve repair: wallerian degeneratioMJG LTn/growth cones. Oper Techn Orthopaed 14: 138-145.
4. Höke A, Redett R, Hameed H, Jari R, Zhou C, et al. (2006) Schwann cells express motor and sensory phenotypes that regulate axon regeneration. J Neurosci 26: 9646-9655.
5. Gordon T, Tyreman N, Raji MA, (2011) The basis for diminished functional recovery after delayed peripheral nerve repair. J Neurosci 31: 5325-5334.
6. Hoyng SA, Tannemaat MR, Winter FD, Verhaagen J, Malessy MJA, (2011) Nerve surgery and gene therapy: a neurobiological and clinical perspective. J Hand Surg Eur 36: 735-746.
7. Midha R, Mackinnon SE, Evans P, Best TJ, Hare GMT, et al. (1993) Comparison of regeneration across nerve allografts with temporary or continuous cyclosporin A immunosuppression. J Neurosurg 78: 90-100.
8. Midha R, Nag S, Munro CA, Ang LC, (2001) Differential response of sensory and motor axons in nerve allografts after withdrawal of immunosuppressive therapy. J Neurosurg 94: 102-110.
9. Wiberg M, Terenghi G, (2003) Will it be possible to produce peripheral nerves? Surg Technol Int 11: 303-310.
10. Schmidt CE, Leach JB, (2003) Neural tissue engineering: strategies for repair and regeneration. Annu Rev Biomed Eng 5: 293-347.
11. Dahlin LB, (2008) Nerve injuries. Curr Orthopaed 22: 9-16.
12. Jiang X, Lim SH, Mao HQ, Chew SY, (2010) Current applications and future perspectives of artificial nerve conduits. Exp Neurol 223: 86-101.
13. Höke A, Brushart TM, (2010) Challenges and opportunities for regeneration in the peripheral nervous system. Exp Neurol 223: 1-4.
14. Madduri S, Gander B, (2010) Schwann cell delivery of neurotrophic factors for peripheral nerve regeneration. J Peripher Nerv Syst 15: 93-103.
15. Gulati AK, Cole GP, (1990) Nerve graft immunogenicity as a factor determining axonal regeneration in the rat. J Neurosurg 72: 114-122.
16. Evans PJ, Mackinnon SE, Levi ADO, Wade JA, Hunter DA, et al. (1998) Cold preserved nerve allografts: changes in basement membrane, viability, immunogenicity, and regeneration. Muscle Nerve 21: 1507-1522.
17. Gulati AK, Rai DR, Ali AM, (1995) The influence of cultured Schwann cells on regeneration through acellular basal lamina grafts. Brain Res 705: 118-124.
18. Cui Q, Pollet MA, Symons NA, Plant GW, Harvey AR, (2003) A new approach to CNS repair using chimeric peripheral nerve grafts. J Neurotrauma 20: 17-31.
19. Frostick SP, Yin Q, Kemp GJ, (1998) Schwann cells, neurotrophic factors, and peripheral nerve regeneration. Microsurgery 18: 398-405.
20. Li Q, Ping P, Jiang H, Liu K, (2005) Nerve conduit filled with GDNF gene-modified Schwann cells enhances regeneration of the peripheral nerve. Microsurgery 26: 116-121.
21. Yu H, Peng J, Guo Q, Zhang L, Li Z, et al. (2009) Improvement of peripheral nerve regeneration in acellular nerve grafts with local release of nerve growth factor. Microsurgery 29: 330-336.
22. Eggers R, Hendriks WT, 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.
23. 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.
24. Hu X, Cai J, Yang J, Smith GM, (2010) Sensory axon targeting is increased by NGF gene therapy within the lesioned adult femoral nerve. Exp Neurol 223: 153-165.
25. 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.
26. Tannemaat MR, Boer GJ, Verhaagen J, Malessy MJA, (2007) Genetic modification of human sural nerve segments by a lentiviral vector encoding Nerve Growth Factor. Neurosurgery 61: 1286-1296.
27. Mason MR, 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.
28. Hu Y, Leaver SG, Plant GW, Hendriks WTJ, Niclou SP, et al. (2005) Lentiviral-mediated transfer of CNTF to Schwann cells within reconstructed peripheral nerve grafts enhances adult retinal ganglion cell survival and axonal regeneration. Mol Ther 11: 906-915.
29. Hu Y, Arulpragasam A, Plant GW, Hendriks WTJ, Cui Q, et al. (2007) The importance of transgene and cell type on the regeneration of adult retinal ganglion cell axons within reconstituted bridging grafts. Exp Neurol 207: 314-328.
30. Hamers FPT, Lankhorst AJ, Laar TJV, Veldhuis WB, Gispen WH, (2001) Automated quantitative gait analysis during overground locomotion in the rat: its application to spinal cord contusion and transection injuries. J Neurotrauma 18: 187-201.
31. Morrissey TK, Kleitman N, Bunge RP, (1991) Isolation and functional characterization of Schwann cells derived from adult peripheral nerve. J Neurosci 11: 2433-2442.
32. Plant GW, Currier PF, Cuervo EP, Bates ML, Pressman Y, et al. (2002) Purified adult ensheathing glia fail to myelinate axons under culture conditions that enable Schwann cells to form myelin. J Neurosci 22: 6083-6091.
33. Symons NA, Danielsen N, Harvey AR, (2001) Migration of cells into and out of peripheral nerve isografts in the peripheral and central nervous systems of the adult mouse. Eur J Neurosci 14: 522-532.
34. Leclere PG, Norman E, Groutsi F, Coffin R, Mayer U, et al. (2007) Impaired axonal regeneration by isolectin B4-binding dorsal root ganglion neurons in vitro. J Neurosci 27: 1190-1199.
35. Augustin-Voss HG, Smith CA, Lewis RM, (1990) Phenotypic characterization of normal and neoplastic canine endothelial cells by lectin histochemistry. Vet Pathol 27: 103-109.
36. Christie KN, Thomson C, (1989) Bandeiraea simplicifolia lectin demonstrates significantly more capillaries in rat skeletal muscle than enzyme methods. J Histochem Cytochem 37: 1303-1304.
37. Ernst C, Christie BR, (2006) Isolectin-IB4 as a vascular stain for the study of adult neurogenesis. J Neurosci Methods 150: 138-142.
38. Pallant J (2007) SPSS survival manual. Crows Nest: Allen & Unwin. 335 p.
39. Nieuwenhuis S, Forstmann BU, Wagenmakers EJ, (2011) Erroneous analyses of interactions in neuroscience: a problem of significance. Nat Neurosci 14: 1105-1107.
40. Bozkurt A, Deumens R, Scheffel J, O'Dey DM, Weis J, et al. (2008) CatWalk gait analysis in assessment of functional recovery after sciatic nerve injury. J Neurosci Methods 173: 91-98.
41. Ju G, Hökfelt T, Brodin E, Fahrenkrug J, Fischer JA, et al. (1987) Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, somatostatin-, galanin-, vasoactive intestinal polypeptide- and cholecystokinin-immunoreactive ganglion cells. Cell Tissue Res 247: 417-431.
42. Murinson BB, Griffin JW, (2004) C-fiber structure varies with location in peripheral nerve. J Neuropathol Exp Neurol 63: 246-254.
43. Nave KA, Schwab MH, (2005) Glial cells under remote control. Nat Neurosci 8: 1420-1422.
44. Griffin JW, Thompson WJ, (2008) Biology and pathology of nonmyelinating Schwann cells. Glia 56: 1518-1531.
45. Gomez-Sanchez JA, Lopez de Armentia M, Lujan R, Kessaris N, Richardson WD, et al. (2009) Sustained axon-glial signaling induces Schwann cell hyperproliferation, remak bundle myelination, and tumorigenesis. J Neurosci 29: 11304-11315.
46. Chomiak T, Hu B, (2009) What is the optimal value of the g-ratio for myelinated fibers in the rat CNS? a theoretical approach. PLoS ONE 4: e7754.
47. Santos PM, Williams SL, Thomas SS, (1995) Neuromuscular evaluation using rat gait analysis. J Neurosci Methods 61: 79-84.
48. Deumens R, Jaken RJP, Marcus MAE, Joosten EAJ, (2007) The CatWalk gait analysis in assessment of both dynamic and static gait changes after adult rat sciatic nerve resection. J Neurosci Methods 164: 120-130.
49. Varejao ASP, Cabrita AM, Geuna S, Melo-Pinto P, Filipe VM, et al. (2003) Toe out angle: a functional index for the evaluation of sciatic nerve recovery in the rat model. Exp Neurol 183: 695-699.
50. Meyer M, Matsuoka I, Wetmore C, Olson L, Thoenen H, (1992) Enhanced synthesis of Brain-derived Neurotrophic Factor in the lesioned peripheral nerve: different mechanisms are responsible for the regulation of BDNF and NGF mRNA. J Cell Biol 119: 45-54.
51. Rabinovsky ED, Smith GM, Browder DP, Shine HD, McManaman JL, (1992) Peripheral nerve injury down-regulates CNTF expression in adult rat sciatic nerves. J Neurosci Res 31: 188-192.
52. Zhang JY, Luo XG, Xian CJ, Liu ZH, Zhou XF, (2000) Endogenous BDNF is required for myelination and regeneration of injured sciatic nerve in rodents. Eur J Neurosci 12: 4171-4180.
53. Xiao J, Wong AW, Willingham MM, Kaasinen SK, Hendry IA, et al. (2009) BDNF exerts contrasting effects on peripheral myelination of NGF-dependent and BDNF-dependent DRG neurons. J Neurosci 29: 4016-4022.
54. Stankoff B, Aigrot MS, Noel F, Wattilliaux A, Zalc B, et al. (2002) Ciliary neurotrophic factor (CNTF) enhances myelin formation: a novel role for CNTF and CNTF-related molecules. J Neurosci 22: 9221-9227.
55. Lang EM, Schlegel CN, Reiners K, Hofmann GO, Sendtner M, et al. (2008) Single-dose application of CNTF and BDNF improves remyelination of regenerating nerve fibers after C7 ventral root avulsion and replantation. J Neurotrauma 25: 384-400.
56. Terenghi G, (1999) Peripheral nerve regeneration and neurotrophic factors. J Anat 194: 1-14.
57. Gordon T, (2009) The role of neurotrophic factors in nerve regeneration. Neurosurg Focus 26: 1-10.
58. Hess DM, Scott MO, Potluri S, Pitts EV, Cisterni C, et al. (2007) Localization of TrkC to Schwann Cells and Effects of Neurotrophin-3 Signaling at Neuromuscular Synapses. J Comp Neurol 501: 465-482.
59. Yamauchi J, Chan JR, Shooter EM, (2003) Neurotrophin 3 activation of TrkC induces Schwann cell migration through the c-Jun N-terminal kinase pathway. Proc Natl Acad Sci U S A 100: 14421-14426.
60. Meier C, Parmantier E, Brennan A, Mirsky R, Jessen KR, (1999) Developing Schwann Cells Acquire the Ability to Survive without Axons by Establishing an Autocrine Circuit Involving Insulin-Like Growth Factor, Neurotrophin-3, and Platelet-Derived Growth Factor-BB. J Neurosci 19: 3847-3859.
61. 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.
62. Sendtner M, Kreutzberg GW, Thoenen H, (1990) Ciliary neurotrophic factor prevents the degeneration of motor neurons after axotomy. Nature 345: 440-441.
63. Ip NY, Yancopoulos GD, (1996) The neurotrophins and CNTF: two families of collaborative neurotrophic factors. Annu Rev Neurosci 19: 491-515.
64. Cen LP, Luo JM, Zhang CW, Fan YM, Song Y, et al. (2007) Chemotactic effect of ciliary neurotrophic factor on macrophages in retinal ganglion cell survival and axonal regeneration. Invest Ophthalmol Vis Sci 48: 4257-4266.
65. Kobayashi H, Mizisin AP, (2000) CNTFRα alone or in combination with CNTF promotes macrophage chemotaxis in vitro. Neuropeptides 34: 338-347.
66. Hoffman PN, (2010) A conditioning lesion induces changes in gene expression and axonal transport that enhance regeneration by increasing the intrinsic growth state of axons. Exp Neurol 223: 11-18.
67. Hoffman PN, Cleveland DW, Griffin JW, Landes PW, Cowan NJ, et al. (1987) Neurofilament gene expression: a major determinant of axonal caliber. Proc Natl Acad Sci U S A 84: 3472-3476.
68. Oblinger MM, Lasek RJ, (1988) Axotomy-induced alterations in the synthesis and transport of neurofilaments and microtubules in dorsal root ganglion cells. J Neurosci 8: 1747-1758.
69. Tetzlaff W, Bisby MA, Kreutzberg GM, (1988) Changes in cytoskeletal proteins in the rat facial nucleus following axotomy. J Neurosci 8: 3181-3189.
70. Moskowitz PF, Oblinger MM, (1995) Sensory neurons selectively upregulate synthesis and transport of the beta III-tubulin protein during axonal regeneration. J Neurosci 15: 1545-1555.
71. Stucky CL, Lewin GR, (1999) Isolectin B4-positive and-negative nociceptors are functionally distinct. J Neurosci 19: 6497-6505.
72. Tucker BA, Rahimtula M, Mearow KM, (2005) A procedure for selecting and culturing subpopulations of neurons from rat dorsal root ganglia using magnetic beads. Brain Res Protoc 16: 50-57.
73. Vulchanova L, Olson TH, Stone LS, Riedl MS, Elde R, et al. (2001) Cytotoxic targeting of isolectin IB4-binding sensory neurons. Neuroscience 108: 143-155.
74. Verge VM, Gratto KA, Karchewski LA, Richardson PM, (1996) Neurotrophins and nerve injury in the adult. Philos Trans R Soc Lond B Biol Sci 351: 423-430.
75. Munson JB, Shelton DL, McMahon SB, (1997) Adult mammalian sensory and motor neurons: roles of endogenous neurotrophins and rescue by exogenous neurotrophins after axotomy. J Neurosci 17: 470-476.
76. Gavazzi I, Kumar RDC, McMahon SB, Cohen J, (1999) Growth responses of different subpopulations of adult sensory neurons to neurotrophic factors in vitro. Eur J Neurosci 11: 3405-3414.
77. New HV, Mudge AW, (1986) Calcitonin-gene related peptide regulates muscle acetylcholine receptor synthesis. Nature 323: 809-811.
78. Zheng LF, Wang R, Xu YZ, Yi XN, Zhang Jian-Wei, et al. (2008) Calcitonin gene-related peptide dynamics in rat dorsal root ganglia and spinal cord following different sciatic nerve injuries. Brain Res 1187: 20-32.
79. Voyvodic JT, (1989) Target size regulates calibre and myelination of sympathetic axons. Nature 342: 430-433.
80. Ng BK, Chen L, Mandemakers W, Cosgaya JM, Chan JR, (2007) Anterograde transport and secretion of Brain-Derived Neurotrophic Factor along sensory axons promote Schwann cell myelination. J Neurosci 27: 7597-7603.
81. Cellerino A, Carroll P, Thoenen H, Barde YA, (1997) Reduced size of retinal ganglion cell axons and hypomyelination in mice lacking Brain-Derived Neurotrophic Factor. Mol Cell Neurosci 9: 397-408.
82. Cosgaya JM, Chan JR, Shooter EM, (2002) The neurotrophin receptor p75NTR as a positive modulator of myelination. Science 298: 1245-1248.
83. Chan JR, Cosgaya JM, Wu YJ, Shooter EM, (2001) Neurotrophins are key mediators of the myelination program in the peripheral nervous system. Proc Natl Acad Sci U S A 98: 14661-14668.
84. Tebar LA, Geranton SM, Parsons-Perez C, Fisher AS, Bayne R, et al. (2008) Deletion of the mouse RegIII (Reg2) gene disrupts ciliary neurotrophic factor signaling and delays myelination of mouse cranial motor neurons. Proc Natl Acad Sci U S A 105: 11400-11405.
85. Medinaceli LD, Freed WJ, Wyatt RJ, (1982) An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks. Exp Neurol 77: 634-643.
86. Decosterd I, Woolf CJ, (2000) Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87: 149-158.
87. Koopmans GC, Deumens R, Honig WMM, Hamers FPT, Steinbusch HWM, et al. (2005) The assessment of locomotor function in spinal cord injured rats: the importance of objective analysis of coordination. J Neurotrauma 22: 214-225.
88. Hamers FPT, Koopmans GC, Joosten EAJ, (2006) CatWalk-assisted gait analysis in the assessment of spinal cord injury. J Neurotrauma 23: 537-548.
89. Costa LM, Simoes MJ, Mauricio AC, Varejao ASP (2009) Kinematic gait analysis to quantify peripheral nerve regeneration in the rat. In: Geuna S, Tos P, Battiston B, editors. Essays on the peripheral nerve repair and regeneration. New York: Academic Press, Elsevier. pp.127-139.
90. Ro LS, Chen ST, Tang LM, Jacobs JM, (1999) Effect of NGF and anti-NGF on neuropathic pain in rats following chronic constriction injury of the sciatic nerve. Pain 79: 265-274.
91. Anand P, (2004) Neurotrophic factors and their receptors in human sensory neuropathies. Prog Brain Res 146: 477-492.
92. Beggs S, Alvares D, Moss A, Currie G, Middleton J, et al. (2012) A role for NT-3 in the hyperinnervation of neonatally wounded skin. Pain 153: 2133-2139.