A spatio-temporal analysis of motoneuron survival, axonal regeneration and neurotrophic factor expression after lumbar ventral root avulsion and implantation

Experimental Neurology

Volumn 223, Issue 1, 2010, Pages 207-220

  Eggers, R ^a   Tannemaat, M R ^b   Ehlert, E M ^a   Verhaagen, J ^a  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Axonal regeneration; Axotomy; Brachial plexus; Denervation; Motoneuron; Neurotrophic factors; Peripheral nerve injury; Ventral root avulsion

Indexed keywords

NEUROTROPHIC FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL SURVIVAL; CONTROLLED STUDY; DENERVATION; FEMALE; GLIA CELL; IMPLANTATION; MOTONEURON; MUSCLE ATROPHY; NERVE REGENERATION; NONHUMAN; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SCIATIC NERVE; SPATIAL SUMMATION; TEMPORAL SUMMATION; VENTRAL ROOT;

ANIMALS; CELL SURVIVAL; CHOLINE O-ACETYLTRANSFERASE; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION REGULATION; HINDLIMB; LUMBOSACRAL PLEXUS; MOTOR NEURONS; MUSCLE, SKELETAL; NERVE GROWTH FACTORS; NERVE REGENERATION; RADICULOPATHY; RATS; RATS, WISTAR; REPLANTATION; SCIATIC NERVE; TIME FACTORS;

EID: 77950866830     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2009.07.021     Document Type: Article

References (71)

1. Aitken J.T., Sharman M., Young J.Z. Maturation of regenerating nerve fibres with various peripheral connexions. J. Anat. 1947, 81:1-22.
2. Asato F., Butler M., Blomberg H., Gordh T. Variation in rat sciatic nerve anatomy: implications for a rat model of neuropathic pain. J. Peripher. Nerv. Syst. 2000, 5:19-21.
3. Aspalter M., Vyas A., Feiner J., Griffin J., Brushart T., Redett R. Modification of Schwann cell gene expression by electroporation in vivo. J. Neurosci. Methods 2009, 176:96-103.
4. Bain J.R., Veltri K.L., Chamberlain D., Fahnestock M. Improved functional recovery of denervated skeletal muscle after temporary sensory nerve innervation. Neuroscience 2001, 103:503-510.
5. Batt J., Bain J., Goncalves J., Michalski B., Plant P., Fahnestock M., Woodgett J. Differential gene expression profiling of short and long term denervated muscle. FASEB J. 2006, 20:115-117.
6. Bergerot A., Shortland P.J., Anand P., Hunt S.P., Carlstedt T. Co-treatment with riluzole and GDNF is necessary for functional recovery after ventral root avulsion injury. Exp. Neurol. 2004, 187:359-366.
7. Bigbee A.J., Hoang T.X., Havton L.A. At-level neuropathic pain is induced by lumbosacral ventral root avulsion injury and ameliorated by root reimplantation into the spinal cord. Exp. Neurol. 2007, 204:273-282.
8. Blesch A., Conner J., Pfeifer A., Gasmi M., Ramirez A., Britton W., Alfa R., Verma I., Tuszynski M.H. Regulated lentiviral NGF gene transfer controls rescue of medial septal cholinergic neurons. Mol. Ther. 2005, 11:916-925.
9. Blits B., Carlstedt T.P., Ruitenberg M.J., de Winter F., Hermens W.T., Dijkhuizen P.A., Claasens J.W., Eggers R., van der S.R., Tenenbaum L., Boer G.J., Verhaagen J. 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. 2004, 189:303-316.
10. Borisov A.B., Dedkov E.I., Carlson B.M. Interrelations of myogenic response, progressive atrophy of muscle fibers, and cell death in denervated skeletal muscle. Anat. Rec. 2001, 264:203-218.
11. Boyd J.G., Gordon T. Neurotrophic factors and their receptors in axonal regeneration and functional recovery after peripheral nerve injury. Mol. Neurobiol. 2003, 27:277-324.
12. Carlstedt T. Root repair review: basic science background and clinical outcome. Restor. Neurol. Neurosci. 2008, 26:225-241.
13. Carlstedt T., Linda H., Cullheim S., Risling M. Reinnervation of hind limb muscles after ventral root avulsion and implantation in the lumbar spinal cord of the adult rat. Acta Physiol. Scand. 1986, 128:645-646.
14. Carlstedt T., Grane P., Hallin R.G., Noren G. Return of function after spinal cord implantation of avulsed spinal nerve roots. Lancet 1995, 346:1323-1325.
15. Carlstedt T., Anand P., Hallin R., Misra P.V., Noren G., Seferlis T. Spinal nerve root repair and reimplantation of avulsed ventral roots into the spinal cord after brachial plexus injury. J. Neurosurg. 2000, 93:237-247.
16. Chai H., Wu W., So K.F., Prevette D.M., Oppenheim R.W. Long-term effects of a single dose of brain-derived neurotrophic factor on motoneuron survival following spinal root avulsion in the adult rat. Neurosci. Lett. 1999, 274:147-150.
17. Chai H., Wu W., So K.F., Yip H.K. Survival and regeneration of motoneurons in adult rats by reimplantation of ventral root following spinal root avulsion. Neuroreport 2000, 11:1249-1252.
18. Cullheim S., Carlstedt T., Risling M. Axon regeneration of spinal motoneurons following a lesion at the cord-ventral root interface. Spinal Cord 1999, 37:811-819.
19. Eggers R., Hendriks W.T., Tannemaat M.R., van Heerikhuize J.J., Pool C.W., Carlstedt T.P., Zaldumbide A., Hoeben R.C., Boer G.J., Verhaagen J. Neuroregenerative effects of lentiviral vector-mediated GDNF expression in reimplanted ventral roots. Mol. Cell. Neurosci. 2008, 39:105-117.
20. Funakoshi H., Frisen J., Barbany G., Timmusk T., Zachrisson O., Verge V.M., Persson H. Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve. J. Cell Biol. 1993, 123:455-465.
21. Fu S.Y., Gordon T. Contributing factors to poor functional recovery after delayed nerve repair: prolonged denervation. J. Neurosci. 1995, 15:3886-3895.
22. Giannini C., Dyck P.J. The fate of Schwann cell basement membranes in permanently transected nerves. J. Neuropathol. Exp. Neurol. 1990, 49:550-563.
23. Gordon T. The role of neurotrophic factors in nerve regeneration. Neurosurg. Focus 2009, 26:E3.
24. Gordon T., Sulaiman O., Boyd J.G. Experimental strategies to promote functional recovery after peripheral nerve injuries. J. Peripher. Nerv. Syst. 2003, 8:236-250.
25. Gu H.Y., Chai H., Zhang J.Y., Yao Z.B., Zhou L.H., Wong W.M., Bruce I., Wu W.T. Survival, regeneration and functional recovery of motoneurons in adult rats by reimplantation of ventral root following spinal root avulsion. Eur. J. Neurosci. 2004, 19:2123-2131.
26. Gu H.Y., Chai H., Zhang J.Y., Yao Z.B., Zhou L.H., Wong W.M., Bruce I.C., Wu W.T. Survival, regeneration and functional recovery of motoneurons after delayed reimplantation of avulsed spinal root in adult rat. Exp. Neurol. 2005, 192:89-99.
27. Hallin R.G., Carlstedt T., Nilsson-Remahl I., Risling M. Spinal cord implantation of avulsed ventral roots in primates; correlation between restored motor function and morphology. Exp. Brain Res. 1999, 124:304-310.
28. Hammarberg H., Piehl F., Cullheim S., Fjell J., Hokfelt T., Fried K. GDNF mRNA in Schwann cells and DRG satellite cells after chronic sciatic nerve injury. Neuroreport 1996, 7:857-860.
29. Hammarberg H., Piehl F., Risling M., Cullheim S. Differential regulation of trophic factor receptor mRNAs in spinal motoneurons after sciatic nerve transection and ventral root avulsion in the rat. J. Comp. Neurol. 2000, 426:587-601.
30. He J.W., Hirata K., Kuraoka A., Kawabuchi M. An improved method for avulsion of lumbar nerve roots as an experimental model of nitric oxide-mediated neuronal degeneration. Brain Res. Brain Res. Protoc. 2000, 5:223-230.
31. Hendriks W.T., Eggers R., Carlstedt T.P., Zaldumbide A., Tannemaat M.R., Fallaux F.J., Hoeben R.C., Boer G.J., Verhaagen J. 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. 2007, 25:585-599.
32. Heumann R., Korsching S., Bandtlow C., Thoenen H. Changes of nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection. J. Cell Biol. 1987, 104:1623-1631.
33. Hoang T.X., Havton L.A. A single re-implanted ventral root exerts neurotropic effects over multiple spinal cord segments in the adult rat. Exp. Brain Res. 2005, 1-10.
34. Hoang T.X., Nieto J.H., Tillakaratne N.J., Havton L.A. Autonomic and motor neuron death is progressive and parallel in a lumbosacral ventral root avulsion model of cauda equina injury. J. Comp. Neurol. 2003, 467:477-486.
35. Hoang T.X., Nieto J.H., Havton L.A. Regenerating supernumerary axons are cholinergic and emerge from both autonomic and motor neurons in the rat spinal cord. Neuroscience 2005, 136:417-423.
36. Hoang T.X., Nieto J.H., Dobkin B.H., Tillakaratne N.J., Havton L.A. Acute implantation of an avulsed lumbosacral ventral root into the rat conus medullaris promotes neuroprotection and graft reinnervation by autonomic and motor neurons. Neuroscience 2006, 138:1149-1160.
37. Hoang T.X., Pikov V., Havton L.A. Functional reinnervation of the rat lower urinary tract after cauda equina injury and repair. J. Neurosci. 2006, 26:8672-8679.
38. Hoke A. Mechanisms of Disease: what factors limit the success of peripheral nerve regeneration in humans?. Nat. Clin. Pract. Neurol. 2006, 2:448-454.
39. Hoke A., Cheng C., Zochodne D.W. Expression of glial cell line-derived neurotrophic factor family of growth factors in peripheral nerve injury in rats. Neuroreport 2000, 11:1651-1654.
40. Hoke A., Gordon T., Zochodne D.W., Sulaiman O.A. A decline in glial cell-line-derived neurotrophic factor expression is associated with impaired regeneration after long-term Schwann cell denervation. Exp. Neurol. 2002, 173:77-85.
41. Hoke A., Redett R., Hameed H., Jari R., Zhou C., Li Z.B., Griffin J.W., Brushart T.M. Schwann cells express motor and sensory phenotypes that regulate axon regeneration. J. Neurosci. 2006, 26:9646-9655.
42. Holmquist B., Kanje M., Kerns J.M., Danielsen N. A mathematical model for regeneration rate and initial delay following surgical repair of peripheral nerves. J. Neurosci. Methods 1993, 48:27-33.
43. Irintchev A., Draguhn A., Wernig A. Reinnervation and recovery of mouse soleus muscle after long-term denervation. Neuroscience 1990, 39:231-243.
44. Jivan S., Novikova L.N., Wiberg M., Novikov L.N. The effects of delayed nerve repair on neuronal survival and axonal regeneration after seventh cervical spinal nerve axotomy in adult rats. Exp. Brain Res. 2006, 170:245-254.
45. Koliatsos V.E., Price W.L., Pardo C.A., Price D.L. Ventral root avulsion: an experimental model of death of adult motor neurons. J. Comp. Neurol. 1994, 342:35-44.
46. Lago N., Navarro X. Correlation between target reinnervation and distribution of motor axons in the injured rat sciatic nerve. J. Neurotrauma 2006, 23:227-240.
47. Li L., Wu W., Lin L.F., Lei M., Oppenheim R.W., Houenou L.J. Rescue of adult mouse motoneurons from injury-induced cell death by glial cell line-derived neurotrophic factor. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:9771-9775.
48. Li L., Xian C.J., Zhong J.H., Zhou X.F. Lumbar 5 ventral root transection-induced upregulation of nerve growth factor in sensory neurons and their target tissues: a mechanism in neuropathic pain. Mol. Cell. Neurosci. 2003, 23:232-250.
49. Malessy M.J., Thomeer R.T. Evaluation of intercostal to musculocutaneous nerve transfer in reconstructive brachial plexus surgery. J. Neurosurg. 1998, 88:266-271.
50. Meyer M., Matsuoka I., Wetmore C., Olson L., Thoenen H. 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. 1992, 119:45-54.
51. Michalski B., Bain J.R., Fahnestock M. Long-term changes in neurotrophic factor expression in distal nerve stump following denervation and reinnervation with motor or sensory nerve. J. Neurochem. 2008, 105:1244-1252.
52. Naveilhan P., ElShamy W.M., Ernfors P. Differential regulation of mRNAs for GDNF and its receptors Ret and GDNFR alpha after sciatic nerve lesion in the mouse. Eur. J. Neurosci. 1997, 9:1450-1460.
53. Nogradi A., Vrbova G. The effect of riluzole treatment in rats on the survival of injured adult and grafted embryonic motoneurons. Eur. J. Neurosci. 2001, 13:113-118.
54. Nogradi A., Szabo A., Pinter S., Vrbova G. Delayed riluzole treatment is able to rescue injured rat spinal motoneurons. Neuroscience 2007, 144:431-438.
55. Novikov L., Novikova L., Kellerth J.O. Brain-derived neurotrophic factor promotes survival and blocks nitric oxide synthase expression in adult rat spinal motoneurons after ventral root avulsion. Neurosci. Lett. 1995, 200:45-48.
56. Omura T., Sano M., Omura K., Hasegawa T., Doi M., Sawada T., Nagano A. Different expressions of BDNF, NT3, and NT4 in muscle and nerve after various types of peripheral nerve injuries. J. Peripher. Nerv. Syst. 2005, 10:293-300.
57. Pan Y.A., Misgeld T., Lichtman J.W., Sanes J.R. Effects of neurotoxic and neuroprotective agents on peripheral nerve regeneration assayed by time-lapse imaging in vivo. J. Neurosci. 2003, 23:11479-11488.
58. Pezet S., McMahon S.B. Neurotrophins: mediators and modulators of pain. Annu. Rev. Neurosci. 2006, 29:507-538.
59. Rende M., Giambanco I., Buratta M., Tonali P. Axotomy induces a different modulation of both low-affinity nerve growth factor receptor and choline acetyltransferase between adult rat spinal and brainstem motoneurons. J. Comp. Neurol. 1995, 363:249-263.
60. Risling M., Sorbye K., Cullheim S. Aberrant regeneration of motor axons into the pia mater after ventral root neuroma formation. Brain Res. 1992, 570:27-34.
61. Shu X.Q., Mendell L.M. Neurotrophins and hyperalgesia. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:7693-7696.
62. Stoll G., Muller H.W. Nerve injury, axonal degeneration and neural regeneration: basic insights. Brain Pathol. 1999, 9:313-325.
63. Sulaiman O.A., Gordon T. Effects of short- and long-term Schwann cell denervation on peripheral nerve regeneration, myelination, and size. Glia 2000, 32:234-246.
64. Sulaiman O.A., Gordon T. Transforming growth factor-beta and forskolin attenuate the adverse effects of long-term Schwann cell denervation on peripheral nerve regeneration in vivo. Glia 2002, 37:206-218.
65. Tannemaat M.R., Eggers R., Hendriks W.T., de Ruiter G.C., van Heerikhuize J.J., Pool C.W., Malessy M.J., Boer G.J., Verhaagen J. 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. 2008, 28:1467-1479.
66. Trupp M., Ryden M., Jornvall H., Funakoshi H., Timmusk T., Arenas E., Ibanez C.F. Peripheral expression and biological activities of GDNF, a new neurotrophic factor for avian and mammalian peripheral neurons. J. Cell Biol. 1995, 130:137-148.
67. Vuorinen V., Siironen J., Roytta M. Axonal regeneration into chronically denervated distal stump. 1. Electron microscope studies. Acta Neuropathol. 1995, 89:209-218.
68. Wu W., Li L. Inhibition of nitric oxide synthase reduces motoneuron death due to spinal root avulsion. Neurosci. Lett. 1993, 153:121-124.
69. Wu W., Han K., Li L., Schinco F.P. Implantation of PNS graft inhibits the induction of neuronal nitric oxide synthase and enhances the survival of spinal motoneurons following root avulsion. Exp. Neurol. 1994, 129:335-339.
70. Xu Q.G., Midha R., Martinez J.A., Guo G.F., Zochodne D.W. Facilitated sprouting in a peripheral nerve injury. Neuroscience 2008, 152:877-887.
71. Zhou L.H., Wu W. Survival of injured spinal motoneurons in adult rat upon treatment with glial cell line-derived neurotrophic factor at 2 weeks but not at 4 weeks after root avulsion. J. Neurotrauma. 2006, 23:920-927.