Use of explant cultures of peripheral nerves of adult vertebrates to study axonal regeneration in vitro

Progress in Neurobiology

Volumn 54, Issue 4, 1998, Pages 459-480

  Tonge, David ^a   Edström, Anders ^b   Ekström, Per ^b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN GEL; PHOSPHOLIPASE A2;

ARTICLE; EXPLANT; FROG; GANGLION; MOUSE; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; PERIPHERAL NERVE; PRIORITY JOURNAL; SENSORY NERVE;

ANIMALS; AXONS; CULTURE TECHNIQUES; NERVE REGENERATION; PERIPHERAL NERVES; VERTEBRATES;

EID: 0032473444     PISSN: 03010082     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0301-0082(97)00072-5     Document Type: Article

References (109)

1. Alvarez E., Northwood I. C., Gonzalez F. A., Latour D. A., Seth A., Abate C., Curran T., Davis R. J. Pro-Leu-Ser/Thr-Pro is a consensus primary sequence for substrate protein phosphorylation. Characterisation of the phosphorylation of c-myc and c-jun proteins by an epidermal growth factor receptor threonine 669 protein kinase. J. Biol. Chem. 266:1991;15277-15285.
2. Ambron R. T., Walters E. T. Priming events and retrograde injury signals: a new perspective on the cellular and molecular biology of nerve regeneration. Mol. Neurobiol. 13:1996;61-79.
3. Averill S., McMahon S. B., Clary D. O., Reichardt L. F., Priestley J. V. Immunocytochemical localisation of trkA receptors in chemically identified subgroups of adult rat sensory neurones. Eur. J. Neurosci. 7:1995;1484-1494.
4. Bailey S. B., Eichler M. E., Villadiego A., Rich K. M. The influence of fibronectin and laminin during Schwann cell migration and peripheral nerve regeneration through silicone chambers. J. Neurocytol. 22:1993;176-184.
5. Barbacid M. Neurotrophic factors and their receptors. Curr. Opin. Cell Biol. 7:1995;148-155.
6. Baron-Van-Evercooren A., Kleinman H. K., Ohno S., Marangos P., Schwartz J. P., Dubois-Dalq M. Nerve growth factor, laminin and fibronectin promote neurite growth in human fetal sensory ganglion cultures. J. Neurosci. 2:1982;179-193.
7. Bedi K. S., Winter J., Berry M. J., Cohen J. Adult rat dorsal root ganglion neurones extend neurites on predegenerated but not on normal peripheral nerves in vitro. Eur. J. Neurosci. 4:1992;193-200.
8. Benowitz L. I., Routtenberg A. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 20:1997;84-91.
9. Bewick G. S., Rowlerson A., Tonge D. A., Holder N. Organisation of motor units in the axolotl: a continuously growing animal. J. Comp. Neurol. 303:1991;551-562.
10. 2+ influx and neurite growth in response to purified N-cadherin and laminin. J. Cell Biol. 127:1994;1461-1475.
11. Brecknell J. E., Fawcett J. W. Axonal regeneration. Biol. Rev. 71:1996;227-255.
12. Brown M. C., Perry V. H., Hunt S. P., Lapper S. R. Further studies on motor and sensory nerve regeneration in mice with delayed Wallerian degeneration. Eur. J. Neurosci. 6:1994;420-428.
13. Buchheit T. E., Tytell M. Transfer of molecules from glia to axon in the squid may be mediated by glial vesicles. J. Neurobiol. 23:1992;217-230.
14. Cabell L., Audesirk G. Effects of selective inhibition of protein kinase c, cyclic AMP-dependent protein kinase, and Ca2+-calmodulin-dependent protein kinase on neurite development in cultured rat hippocampal neurones. Int. J. Devl. Neurosci. 11:1993;357-368.
15. Campenot R. B., Draker D. D., Senger D. L. Evidence that protein kinase c activities involved in regulating neurite growth are localised to distal neurites. J. Neurochem. 63:1994;868-878.
16. Carbonetto S. The extracellular matrix of the nervous system. Trends Neurosci. 7:1994;382-387.
17. Davies, A. M. (1989) Neurotrophic factor bioassay using dissociated neurones. In: Nerve Growth Factors, pp. 95-109. Ed. R. Rush. Wiley: New York.
18. Derby A., Engleman V. W., Frierdich G. E., Neises G., Rapp S. R., Roufa D. G. Nerve growth factor facilitates regeneration across nerve gaps: morphological and behavioural studies in rat sciatic nerve. Exp. Neurol. 119:1993;176-191.
19. Doherty P., Walsh F. S. Signal transduction events underlying neurite outgrowth stimulated by cell adhesion molecules. Curr. Opin. Neurobiol. 4:1994;49-55.
20. Doherty P., Ashton S. V., Moore S. E., Walsh F. S. Morphoregulatory activities of NCAM and N-cadherin can be accounted for by G protein-dependent activation of L- and N-type neuronal Ca2+ channels. Cell. 67:1991;21-33.
21. Doyu M., Sobue G., Ken E., Kimata K., Shinomura T., Yamada Y., Mitsuma T., Takahashi A. Laminin A, B1 and B2 chain gene expression in transected and regenerating nerves: regulation by axonal signals. J. Neurochem. 60:1993;543-551.
22. Durbec P., Marcos-Gutierrez C. V., Kilkenny C., Grigoriou M., Wartiowaara K., Suvanto P., Smith D., Ponder B., Constantini F., Saarma M., Sariola H., Pachnis V. GDNF signalling through the Ret receptor tyrosine kinase. Nature. 381:1996;789-793.
23. Ebendal, T. (1989) Use of collagen gels to bioassay nerve growth factor activity. In: Nerve Growth Factors, pp. 81-93. Ed. R. Rush. Wiley: New York.
24. Edbladh M., Ekström P. A. R., Edström A. Retrograde transport of locally synthesised proteins e.g. actin and heat shock protein 70, in regenerating adult frog sensory axons. J. Neurosci. Res. 38:1994;424-432.
25. Edbladh M., Remgård P., Edström A. A new method to study regeneration in vitro of the adult frog sciatic sensory axons. J. Neurosci. Meths. 32:1990;1-7.
26. Edbladh M., Tonge D. A., Golding J., Ekström P. A. R., Edström A. Early regeneration in vitro of adult mouse sciatic axons is dependent on local protein synthesis but may not involve neurotrophins. Neurosci. Letts. 168:1994;37-40.
27. Edström A., Briggman M., Ekström P. A. R. Phospholipase A2 activity is required for regeneration of sensory axons in cultured adult sciatic nerves. J. Neurosci. Res. 43:1996;183-189.
28. Edström A., Edbladh M., Ekström P., Remgård P. Regeneration in vitro of the adult frog sciatic sensory axons. Restor. Neurol. Neurosci. 1:1990;261-266.
29. Edström A., Ekström P. A. R., Tonge D. A. Axonal outgrowth and neuronal apoptosis in cultured adult mouse DRG preparations: effects of neurotrophins, of inhibition of neurotrophin actions, and of prior axotomy. Neurosci. 75:1996;1165-1174.
30. Edström A., Kanje M. Regeneration in vitro of the adult frog sciatic nerve. Neurosci. Letts. 90:1988;113-118.
31. Edström A., Mattsson H. Electrophoretic characterisation of leucine-, glucosamine- and fucose-labelled proteins rapidly transported in frog sciatic nerve. J. Neurochem. 21:1973;1499-1509.
32. Edström A., Sjöberg J., Kanje M. The use of whole-mount preparations of nerves labelled with axonally transported radioactive proteins to study axonal regeneration. J. Neurosci. Methods. 16:1986;19-27.
33. Ekström P. A. Neurones and glial cells of the mouse sciatic nerve undergo apoptosis after injury in vivo and in vitro. Neuroreport. 6:1995;1029-1032.
34. Fawcett J. W., Keynes R. J. Peripheral nerve regeneration. Annu. Rev. Neurosci. 13:1990;43-60.
35. Felipo V., Miñana M.-D., Grisolia S. A specific inhibitor of protein kinase c induces differentiation of neuroblastoma cells. J. Biol. Chem. 265:1990;9599-9601.
36. Funakoshi H., Frisén J., Barnaby G., Timmusk T., Zachrisson O., Verge V. M. K., Persson H. Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve. J. Cell Biol. 123:1993;455-465.
37. Gille H., Sharrocks A. D., Shaw P. E. Phosphorylation of transcription factor P62T-C-F by MAP kinase stimulates ternary complex formation at c-fos promoter. Nature. 358:1992;414-417.
38. Gold B. G., Storm-Dickerson T., Austin D. R. The immunosuppressant FK506 increases functional recovery and nerve regeneration following peripheral nerve injury. Restor. Neurol. Neurosci. 6:1994;287-296.
39. Hall S. M. The effect of inhibiting Schwann cell mitosis on the re-innervation of acellular autografts in the peripheral nervous system of the mouse. Neuropath. Appl. Neurobiol. 12:1986;401-414.
40. Hall F. L., Fernyhough P., Ishii D. N., Vulliet P. R. Suppression of nerve growth factor-directed neurite outgrowth in PC12 cells by sphingosine, an inhibitor of protein kinase C. J. Biol. Chem. 263:1987;4460-4466.
41. Harris A. J., Miledi R. Prolonged survival of isolated frog muscle and its sensitivity to acetylcholine. Nature. 209:1966;716-717.
42. Hayden S. M., Seeds N. W. Modulated expression of plasminogen activator system components in cultured cells from dissociated mouse dorsal root ganglia. J. Neurosci. 16:1996;2307-2317.
43. Herbert J. M., Augereau J. M., Gleye J., Maffrand J. P. Chelerythrine is a potent and specific inhibitor of protein kinase C. Biochem. Biophys. Res. Commun. 172:1990;993-999.
44. Hidaka H., Inagaki M., Kawamoto S., Sasaki Y. Isoquinoline-sulphonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. Biochemistry. 23:1984;5036-5041.
45. Hoffman P. M., Luduena R. F. Changes in the isotype composition of beta-tubulin delivered to regenerating axons by slow axonal transport. Brain Res. 742:1996;329-333.
46. Holder N., Clarke J. D. W., Stephens N., Wilson S. W., Orci C., Bloomer T., Tonge D. A. Continuous growth of the motor system in the axolotl. J. Comp. Neurol. 303:1991;534-550.
47. Holder N. H. K., Mills J., Tonge D. A. Mechanisms involved in selective reinnervation of skeletal muscle in the newt. J. Physiol. 326:1982;371-384.
48. Holder N., Tonge D. A., Jesani P. Directed regrowth of axons from a misrouted nerve to their correct muscles in the limb of the adult newt. Proc. R. Soc. B. 222:1984;477-484.
49. Houenou L. J., Li L., Lei M., Kent C. R., Tytell M. Exogenous heat shock cognate protein Hsc70 prevents axotomy-induced death of spinal sensory neurones. Cell Stress and Chaperones. 1:1996;161-166.
50. Hu-Tsai M., Winter J., Emson P. C., Woolf C. J. Neurite outgrowth and GAP 43 expression in cultured adult rat dorsal root ganglion neurones: effects of NGF or prior peripheral axotomy. J. Neurosci. Res. 39:1994;634-645.
51. Jian X., Hidaka H., Schmidt J. T. Kinase requirement for retinal growth cone motility. J. Neurobiol. 25:1994;1310-1328.
52. Jing S., Wen D., Yu Y., Hoist P. L., Luo Y., Fang M., Tamir R., Antonio L., Hu Z., Cupples R., Louis J. C., Hu S., Altrock B. W., Fox G. M. GDNF-induced activation of the ret protein tyrosine kinase is mediated by GDNF-alpha, a novel receptor for GDNF. Cell. 85:1966;1113-1124.
53. Kanje M. Survival and regeneration of the adult rat vagus nerve in culture. Brain Res. 550:1991;340-342.
54. Kanje M. Regeneration of an adult peripheral nerve preparation in culture. Mol. Neurobiol. 6:1992;217-223.
55. Kanje M., Skottner A., Sjöberg J., Lundborg G. Insulin-like growth factor 1 (IGF-1) stimulates regeneration of the rat sciatic nerve. Brain Res. 486:1989;396-398.
56. Kleinman H. K., McGarvey M. L., Hassell J. R., Star V. L., Cannon F. B., Laurie G. L., Martin G. R. Basement membrane complexes with biological activity. Biochemistry. 25:1986;312-318.
57. Krystosek A., Seeds N. W. Plasminogen activator release at the neuronal growth cone. Science. 213:1981;1532-1534.
58. Laird J. M. A., Mason G. S., Thomas K. A., Hargreaves R. J., Hill R. G. Acidic fibroblast growth factor stimulates motor and sensory axon regeneration after sciatic nerve crush in the rat. Neurosci. 65:1995;209-216.
59. Lander A. D. Molecules that make axons grow. Mol. Neurobiol. 1:1987;213-245.
60. Lander A. D., Fujii D. K., Reichardt L. F. Laminin is associated with "neurite outgrowth-promoting factors" found in conditioned media. Proc. Natl. Acad. Sci. (USA). 82:1985;2183-2187.
61. Lasek, R. J. and Tytell, M. A. (1981) Macromolecular transfer from glia to the axon. J. Exp. Biol., 95, 153-165.
62. Lawson S. N., Perry M. J., Prabhaker E., McCarthy P. W. Primary sensory neurones: neurofilament, neuropeptides and conduction velocity. Brain Res. Bull. 30:1993;239-243.
63. Leclere, P., Ekström, P., Edström, A., Priestley, J., Averill, S. and Tonge, D. A. (1997) Effects of glial cell line-derived neurotrophic factor on axonal growth and apoptosis in adult mammalian sensory neurones in vitro. Neurosci., 82, 545-558.
64. Lewin G. R., Rueff A., Mendell L. M. Peripheral and central mechanisms of NGF-induced hyperalgesia. Eur. J. Neurosci. 6:1994;1903-1912.
65. Lindholm D., Heumann R., Meyer M., Thoenen H. Interleukin-1 regulates synthesis of nerve growth factor in non-neuronal cells of rat sciatic nerve. Nature. 330:1987;658-659.
66. Lindsay R. M. Nerve growth factors (NGF, BDNF) enhance axonal regeneration but are not required for survival of adult sensory neurones. J. Neurosci. 8:1988;2394-2408.
67. Lindsay, R. M. (1992) The role of neurotrophic factors in functional maintenance of mature sensory neurones. In: Sensory Neurones. Development, Diversity, and Plasticity, pp. 404-420. Ed. S. A. Scott. Oxford University Press: New York.
68. Lundborg, G. (1988) Nerve Injury and Repair. Churchill Livingstone: Edinburgh.
69. Lyons W. E., George E. B., Dawson T. M., Steiner J. P., Snider S. H. Immunosuppressant FK506 promotes neurite outgrowth in cultures of PC 12 cells and sensory ganglia. Proc. Natl Acad. Sci. (USA). 91:1994;3191-3195.
70. Malgrange B., Delree P., Rigo J. M., Baron H., Moonen G. Image analysis of neuritic regeneration by adult rat dorsal root ganglion neurones in culture: quantitation of the neurotoxicity of anticancer agents and of its prevention by nerve growth factor or basic fibroblast growth factor but not by brain-derived neurotrophic factor or neurotrophin-3. J. Neurosci. Methods. 53:1994;111-122.
71. Martini R. Expression and functional roles of neural cell surface molecules and extracellular matrix components during development and regeneration of peripheral nerves. J. Neurocytol. 23:1994;1-28.
72. McFarlane S., McNeill L., Holt C. E. FGF signalling and target recognition in the developing Xenopus visual system. Neuron. 15:1995;1017-1028.
73. Meyer M., Matsuoka I., Wetmore C., Olsen 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. 119:1992;45-54.
74. Michael, G. J., Klein, R. D., Phillips, H. S. and Priestley, J. V. (1997) Expression of mRNAs for RET, GDNFR-α and NTNR-α in identified rat lumbar DRG cell populations. Soc. Neurosci. Abs 23.
75. Miñana M.-D., Felipo V., Grisolja S. Inhibition of protein kinase c induces differentiation in neuro-2a cells. Proc. Natl. Acad. Sci. (USA). 87:1990;4335-4339.
76. Molliver D. C., Radeke M. J., Feinstein S. C., Snider W. D. Presence or absence of trkA protein distinguishes subsets of small sensory neurones with unique cytochemical characteristics and dorsal horn projections. J. Comp. Neurol. 361:1995;404-416.
77. Monard D. Cell-derived proteases and protease inhibitors as regulators of neurite outgrowth. Trends Neurosci. 11:1988;541-544.
78. Mukhopadhyay G., Doherty P., Walsh F. S., Crocker P. R., Filbin M. T. A novel role for myelin-associated glycoprotein as an inhibitor of axonal regeneration. Neuron. 13:1994;757-767.
79. Muir D. Metalloprotease-dependent neurite outgrowth within a synthetic extracellular matrix is induced by nerve growth factor. Exp. Cell Res. 210:1994;243-252.
80. Nicosia R. F., Ottinetti A. Growth of microvessels in serum-free matrix cultures of rat aorta. Lab. Invest. 63:1990;115-122.
81. Olsen C. L., Bunge R. P. Requisites for growth and myelination of urodele sensory neurons in tissue culture. J. Exp. Zool. 238:1986;273-284.
82. Puelve P., Laquerriere A., Paresy M., Hemet J., Tadie M. Establishment of adult rat Schwann cell cultures: effect of b-FGF, alpha-MSH, NGF, PDGF, and TGF-beta on cell cycle. Exp. Cell Res. 214:1994;543-550.
83. Pulverer B. J., Kyriakis J. M., Avruch J., Nikolakaki E., Woodgett J. R. Phosphorylation of c-Jun mediated by MAP kinases. Nature. 353:1991;670-674.
84. Ray L. B., Sturgill T. W. Rapid stimulation by insulin of a serine/threonine kinase in 3T3-L1 adipocytes that phosphorylates microtubule-associated protein 2 in vitro. Proc. Natl. Acad. Sci. (USA). 84:1987;1502-1506.
85. Remgård P., Edbladh M., Ekström P. A. R., Edström A. Growth cones of regenerating adult sciatic sensory axons release axonally transported proteins. Brain Res. 572:1992;139-145.
86. Sekel B. R. Enhancement of peripheral nerve regeneration. Muscle Nerve. 13:1990;785-800.
87. Shea T. B., Beermann M. L., Leli U., Nixon R. A. Opposing influences of protein kinase activities on neurite outgrowth in human neuroblastoma cells: initiation by kinase A and restriction by kinase C. J. Neurosci. Res. 33:1992;398-407.
88. Shy M. E., Shi Y., Wrabez L., Kambolz J., Scherer S. S. Axon-Schwann cell interactions regulate the expression of c-jun in Schwann cells. J. Neurosci. Res. 43:1996;511-525.
89. Skene J. H. P. Axonal growth-associated proteins. Annu. Rev. Neurosci. 12:1989;127-156.
90. Smith D. S., Skene J. H. P. A transcription-dependent switch controls competence of adult neurons for distinct modes of axon growth. J. Neurosci. 17:1997;646-658.
91. Stewart H. J. Expression of c-Jun, Jun B, Jun D and cAMP response element binding protein by Schwann cells and their precursors in vivo and in vitro. Eur. J. Neurosci. 7:1995;1366-1375.
92. Stone G. C., Hammerschlag R. Glycosylation as a criterion for defining subpopulations of fast-transported proteins. J. Neurochem. 40:1983;1124-1133.
93. Sumner A. J. Aberrant innervation. Muscle Nerve. 13:1990;801-803.
94. Svensson B., Ekström P. A. R., Edström A. Increased levels of mitogen activated protein kinase (MAP-K) detected in the injured adult mouse sciatic nerve. Neurosci. Letts. 200:1995;33-36.
95. Tessier-Lavigne M., Goodman C. S. The molecular biology of axon guidance. Science. 274:1996;1123-1133.
96. Tapley P., Lamballe F., Barbacid M. K252a is a selective inhibitor of the tyrosine protein kinase activity of the trk family of oncogenes and neurotrophin receptors. Oncogene. 7:1992;371-381.
97. Thomas P. K. Focal nerve injury: guidance factors during axonal regeneration. Muscle and Nerve. 12:1989;796-802.
98. Tonge D. A., Aaronson O. S., Golding J. P., Jaggers D. Cellular migration and axonal outgrowth from adult mammalian peripheral nerves in vitro. J. Neurobiol. 29:1996;151-164.
99. Tonge D. A., Clarke J. D. W., Hunter K., Golding J. Regeneration in vitro of axolotl peripheral and central axons. Restor. Neurol. Neurosci. 1:1990;267-273.
100. Tonge D. A., Golding J. P., Edbladh M., Kroon M., Ekström P. A. R., Edström A. Effects of extracellular matrix components on axonal outgrowth from peripheral nerves of adult animals in vitro. Exp. Neurol. 146:1997;81-90.
101. Tonge D. A., Golding J. P., Gordon-Weeks P. R. Expression of a developmentally regulated, phosphorylated isoform of microtubule-associated protein 1B in sprouting and regenerating axons in vitro. Neurosci. 73:1996;541-551.
102. Tonge D. A., Leclere P. G. Diffusible factors from axolotl blastemas stimulate axonal growth. Brain Res. Assoc. Abstr. 14:1997;45.
103. Trupp M., Rydén M., Jörnvall H., Funakoshi H., Timmusk T., Arenas E., Ibanéz C. F. Peripheral expression and biological activities of GDNF, a new neurotrophic factor for avian and mammalian peripheral neurons. J. Cell Biol. 130:1995;137-148.
104. van Deenen L. L. M., de Haas G. H. The substrate specificity of phospholipase A. Biochim. Biophys. Acta. 70:1963;538-553.
105. Vukicevic S., Kleinman H. K., Luyten F. P., Roberts V., Roche N. S., Reddi A. H. Identification of multiple active growth factors in basement membrane Matrigel suggests caution in interpretation of cellular activity related to extracellular matrix components. Exp. Cell Res. 202:1992;1-8.
106. Welch W. J. Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol. Rev. 72:1992;1063-1081.
107. Wiklund P., Ekström P. A. R., Edbladh M., Tonge D., Edström A. Protein kinase C and mouse sciatic nerve regeneration. Brain Res. 715:1994;145-154.
108. Wigston D. J., Kennedy P. R. Selective reinnervation of transplanted muscles by their original motoneurons in the axolotl. J. Neurosci. 7:1987;1857-1865.
109. Wilson P. O. G., Barber P. C., Hamid Q. A., Power B. F., Dhillon A. P., Rhode J., Day I. N. M., Thompson R. J., Polak J. M. Immunolocalization of protein gene product 9.5 using rabbit polyclonal and mouse monoclonal antibodies. Br. J. Exp. Path. 69:1988;91-104.