Intrinsic neuronal properties control selective targeting of regenerating motoneurons

Brain

Volumn 131, Issue 6, 2008, Pages 1492-1505

  Franz, Colin K ^a   Rutishauser, Urs ^b   Rafuse, Victor F ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Axon guidance; Electrical stimulation; NCAM; Polysialic acid; Sprouting

Indexed keywords

POLYSIALIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ELECTROSTIMULATION; FEMORAL NERVE; MALE; MOTONEURON; MOUSE; MUSCLE REINNERVATION; NERVE FIBER REGENERATION; NERVE FUNCTION; NERVE SPROUTING; NERVE SUTURE; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL;

EID: 44949147987     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awn039     Document Type: Article

References (71)

1. Abercrombie M. Estimation of nuclear population from microtome sections. Anat Neurobiol Rec 1946; 94: 239-47.
2. Ahlborn P, Schachner M, Irintchev A. One hour electrical stimulation accelerates functional recovery after femoral nerve repair. Exp Neurol 2007; 208: 137-44.
3. Al-Majed AA, Brushart TM, Gordon T. Electrical stimulation accelerates and increases expression of BDNF and trkB mRNA in regenerating rat femoral motoneurons. Eur J Neurosci 2000a; 12: 4381-90.
4. Al-Majed AA, Neumann CM, Brushart TM, Gordon T. Brief electrical stimulation promotes the speed and accuracy of motor axonal regeneration. J Neurosci 2000b; 20: 2602-8.
5. Al-Majed AA, Tam SL, Gordon T. Electrical stimulation accelerates and enhances expression of regeneration-associated genes in regenerating rat femoral motoneurons. Cell Mol Neurobiol 2004; 24: 379-402.
6. Allan DW, Greer JJ. Polysialylated NCAM expression during motor axon outgrowth and myogenesis in the fetal rat. J Comp Neurol 1998; 391: 275-92.
7. Bosse F, Hasenpusch-Theil K, Kury P, Muller HW. Gene expression profiling reveals that peripheral nerve regeneration is a consequence of both novel injury-dependent and reactivated developmental processes. J Neurochem 2006; 96: 1441-57.
8. Brushart TM. Preferential reinnervation of motor nerves by regenerating motor axons. J Neurosci 1988; 8: 1026-31.
9. Brushart TM. Motor axons preferentially reinnervate motor pathways. J Neurosci 1993; 13: 2730-8.
10. Brushart TM, Gerber J, Kessens P, Chen YG, Royall RM. Contributions of pathway and neuron to preferential motor reinnervation. J Neurosci 1998; 18: 8674-81.
11. Brushart TM, Hoffman PN, Royall RM, Murinson BB, Witzel C, Gordon T. Electrical stimulation promotes motoneuron regeneration without increasing its speed or conditioning the neuron. J Neurosci 2002; 22: 6631-8.
12. Bukalo O, Fentrop N, Lee AY, Salmen B, Law JW, Wotjak CT, et al. J Neurosci 2004; 24: 1565-77.
13. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, Roes J, et al. Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 1994; 367: 455-9.
14. Eberhardt KA, Irintchev A, Al-Majed AA, Simova O, Brushart TM, Gordon T, et al. BDNF/TrkB signaling regulates HNK-1 carbohydrate expression in regenerating motor nerves and promotes functional recovery after peripheral nerve repair. Exp Neurol 2006; 198: 500-10.
15. El Maarouf A, Rutishauser U. Removal of polysialic acid induces aberrant pathways, synaptic vesicle distribution, and terminal arborization of retinotectal axons. J Comp Neurol 2003; 460: 203-11.
16. English AW. Enhancing axon regeneration in peripheral nerves also increases functionally inappropriate reinnervation of targets. J Comp Neurol 2005; 490: 427-41.
17. English AW, Schwartz G, Meador W, Sabatier MJ, Mulligan A. Electrical stimulation promotes peripheral axon regeneration by enhanced neuronal neurotrophin signaling. Dev Neurobiol 2007; 67-72.
18. Franz CK, Rutishauser U, Rafuse VF. Polysialylated neural cell adhesion molecule is necessary for selective targeting of regenerating motor neurons. J Neurosci 2005; 25: 2081-91.
19. Fu M, Vohra BP, Wind D, Heuckeroth RO. BMP signaling regulates murine enteric nervous system precursor migration, neurite fasciculation, and patterning via altered Ncam1 polysialic acid addition. Dev Biol 2006; 299: 137-50.
20. Gascon E, Vutskits L, Jenny B, Durbec P, Kiss JZ. PSA-NCAM in postnatally generated immature neurons of the olfactory bulb: a crucial role in regulating p75 expression and cell survival. Development 2007; 134: 1181-90.
21. Geremia NM, Gordon T, Brushart TM, Al-Majed AA, Verge VM. Electrical stimulation promotes sensory neuron regeneration and growth-associated gene expression. Exp Neurol 2007; 205: 347-59.
22. Goldberg JL. Intrinsic neuronal regulation of axon and dendrite growth. Curr Opin Neurobiol 2004; 14: 551-7.
23. Hanson MG, Landmesser LT. Normal patterns of spontaneous activity are required for correct motor axon guidance and the expression of specific guidance molecules. Neuron 2004; 43: 687-701.
24. Hanson MG, Landmesser LT. Increasing the frequency of spontaneous rhythmic activity disrupts pool-specific axon fasciculation and pathfinding of embryonic spinal motoneurons. J Neurosci 2006; 26: 12769-80.
25. Helmbacher F, Schneider-Maunoury S, Topilko P, Tiret L, Charnay P. Targeting of the EphA4 tyrosine kinase receptor affects dorsal/ventral pathfinding of limb motor axons. Development 2000; 127: 3313-24.
26. Hess DM, Scott MO, Potluri S, Pitts EV, Cisterni C, Balice-Gordon RJ. Localization of TrkC to Schwann cells and effects of neurotrophin-3 signaling at neuromuscular synapses. J Comp Neurol 2007; 501: 465-82.
27. Hoke A, Redett R, Hameed H, Jari R, Zhou C, Li ZB, et al. Schwann cells express motor and sensory phenotypes that regulate axon regeneration. J Neurosci 2006; 26: 9646-55.
28. Itoh K, Stevens B, Schachner M, Fields RD. Regulated expression of the neural cell adhesion molecule L1 by specific patterns of neural impulses. Science 1995; 270: 1369-72.
29. Jones CL. The morphogenesis of the thigh of the mouse with special reference to tetrapod muscle homologies. J Morphol 1979; 162: 275-309.
30. Kiss JZ, Wang C, Olive S, Rougon G, Lang J, Baetens D, et al. Activity-dependent mobilization of the adhesion molecule polysialic NCAM to the cell surface of neurons and endocrine cells. Embo J 1994; 13: 5284-92.
31. Krarup C, Archibald SJ, Madison RD. Factors that influence peripheral nerve regeneration: an electrophysiological study of the monkey median nerve. Ann Neurol 2002; 51: 69-81.
32. Landmesser L, Dahm L, Schultz K, Rutishauser U. Distinct roles for adhesion molecules during innervation of embryonic chick muscle. Dev Biol 1988; 130: 645-70.
33. Landmesser LT. The acquisition of motoneuron subtype identity and motor circuit formation. Int J Dev Neurosci 2001; 19: 175-82.
34. Livet J, Sigrist M, Stroebel S, De Paola V, Price SR, Henderson CE, et al. ETS gene Pea3 controls the central position and terminal arborization of specific motor neuron pools. Neuron 2002; 35: 877-92.
35. Mackinnon SE, Dellon AL. Surgery of the peripheral nerve. New York: Thieme Medical Publishers, Inc.; 1988.
36. Madison RD, Archibald SJ, Brushart TM. Reinnervation accuracy of the rat femoral nerve by motor and sensory neurons. J Neurosci 1996; 16: 5698-703.
37. Madison RD, Archibald SJ, Lacin R, Krarup C. Factors contributing to preferential motor reinnervation in the primate peripheral nervous system. J Neurosci 1999; 19: 11007-16.
38. Madison RD, Robinson GA, Chadaram SR. The specificity of motor neurone regeneration (preferential reinnervation). Acta Physiol (Oxf) 2007; 189: 201-6.
39. Maehlen J, Nja A. The effects of electrical stimulation on sprouting after partial denervation of guinea-pig sympathetic ganglion cells. J Physiol 1982; 322: 151-66.
40. Manivannan S, Terakawa S. Rapid sprouting of filopodia in nerve terminals of chromaffin cells, PC12 cells, and dorsal root neurons induced by electrical stimulation. J Neurosci 1994; 14: 5917-28.
41. Martini R, Schachner M, Brushart TM. The L2/HNK-1 carbohydrate is preferentially expressed by previously motor axon-associated Schwann cells in reinnervated peripheral nerves. J Neurosci 1994; 14: 7180-91.
42. Martini R, Xin Y, Schmitz B, Schachner M. The L2/HNK-1 carbohydrate epitope is involved in the preferential outgrowth of motor neurons on ventral roots and motor nerves. Eur J Neurosci 1992; 4: 628-39.
43. Mears S, Schachner M, Brushart TM. Antibodies to myelin-associated glycoprotein accelerate preferential motor reinnervation. J Peripher Nerv Syst 2003; 8: 91-9.
44. Nguyen QT, Sanes JR, Lichtman JW. Pre-existing pathways promote precise projection patterns. Nat Neurosci 2002; 5: 861-7.
45. Nix WA, Hopf HC. Electrical stimulation of regenerating nerve and its effect on motor recovery. Brain Res 1983; 272: 21-5.
46. Pockett S, Gavin RM. Acceleration of peripheral nerve regeneration after crush injury in rat. Neurosci Lett 1985; 59: 221-4.
47. Price SR, De Marco Garcia NV, Ranscht B, Jessell TM. Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 2002; 109: 205-16.
48. Rafuse VF, Landmesser L. Contractile activity regulates isoform expression and polysialylation of NCAM in cultured myotubes: involvement of Ca2+ and protein kinase C. J Cell Biol 1996; 132: 969-83.
49. Ramon y Cajal S. Degeneration and regeneration of the nervous sytem. London: Oxford University Press; 1928.
50. Redett R, Jari R, Crawford T, Chen YG, Rohde C, Brushart TM. Peripheral pathways regulate motoneuron collateral dynamics. J Neurosci 2005; 25: 9406-12.
51. Robinson GA, Madison RD. Preferential motor reinnervation in the mouse: comparison of femoral nerve repair using a fibrin sealant or suture. Muscle Nerve 2003; 28: 227-31.
52. Robinson GA, Madison RD. Motor neurons can preferentially reinnervate cutaneous pathways. Exp Neurol 2004; 190: 407-13.
53. Robinson GA, Madison RD. Manipulations of the mouse femoral nerve influence the accuracy of pathway reinnervation by motor neurons. Exp Neurol 2005; 192: 39-45.
54. Rossi F, Gianola S, Corvetti L. Regulation of intrinsic neuronal properties for axon growth and regeneration. Prog Neurobiol 2007; 81: 1-28.
55. Rutishauser U. Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat Rev Neurosci 2008; 9: 26-35.
56. Sanes JR, Marshall LM, McMahan UJ. Reinnervation of muscle fiber basal lamina after removal of myofibers. Differentiation of regenerating axons at original synaptic sites. J Cell Biol 1978; 78: 176-98.
57. Schafer M, Fruttiger M, Montag D, Schachner M, Martini R. Disruption of the gene for the myelin-associated glycoprotein improves axonal regrowth along myelin in C57BL/Wlds mice. Neuron 1996; 16: 1107-13.
58. Simon M, Mann D, Coulton G, Terenghi G. Differential tyrosine kinase C mRNA distribution in extensor digitorum longus and soleus motoneurons in adult rats: effect of axotomy and neurotrophin-3 treatment. Neurosci Lett 2002; 320: 9-12.
59. Song MR, Pfaff SL. Hox genes: the instructors working at motor pools. Cell 2005; 123: 363-5.
60. Soundararajan P, Miles GB, Rubin LL, Brownstone RM, Rafuse VF. Motoneurons derived from embryonic stem cells express transcription factors and develop phenotypes characteristic of medial motor column neurons. J Neurosci 2006; 26: 3256-68.
61. Sunderland S. Nerve and nerve injuries. New York: Churchill Livingstone; 1978.
62. Tang J, Landmesser L, Rutishauser U. Polysialic acid influences specific pathfinding by avian motoneurons. Neuron 1992; 8: 1031-44.
63. Tang J, Rutishauser U, Landmesser L. Polysialic acid regulates growth cone behavior during sorting of motor axons in the plexus region. Neuron 1994; 13: 405-14.
64. Uschold T, Robinson GA, Madison RD. Motor neuron regeneration accuracy: balancing trophic influences between pathways and endorgans. Exp Neurol 2007; 205: 250-6.
65. Vimr ER, McCoy RD, Vollger HF, Wilkison NC, Troy FA. Use of prokaryotic-derived probes to identify poly(sialic acid) in neonatal neuronal membranes. Proc Natl Acad Sci USA 1984; 81: 1971-5.
66. Vutskits L, Djebbara-Hannas Z, Zhang H, Paccaud JP, Durbec P, Rougon G, et al. PSA-NCAM modulates BDNF-dependent survival and differentiation of cortical neurons. Eur J Neurosci 2001; 13: 1391-402.
67. Vutskits L, Gascon E, Kiss JZ. Removal of PSA from NCAM affects the survival of magnocellular vasopressin- and oxytocin-producing neurons in organotypic cultures of the paraventricular nucleus. Eur J Neurosci 2003; 17: 2119-26.
68. Wichterle H, Lieberam I, Porter JA, Jessell TM. Directed differentiation of embryonic stem cells into motor neurons. Cell 2002; 110: 385-97.
69. Wilson JM, Hartley R, Maxwell DJ, Todd AJ, Lieberam I, Kaltschmidt JA, et al. Conditional rhythmicity of ventral spinal interneurons defined by expression of the Hb9 homeodomain protein. J Neurosci 2005; 25: 5710-9.
70. Witzel C, Rohde C, Brushart TM. Pathway sampling by regenerating peripheral axons. J Comp Neurol 2005; 485: 183-90.
71. Yang X, Arber S, William C, Li L, Tanabe Y, Jessell TM, et al. Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 2001; 30: 399-410.