Effects of glial cell line-derived neurotrophic factor on axonal growth and apoptosis in adult mammalian sensory neurons in vitro

Neuroscience

Volumn 82, Issue 2, 1997, Pages 545-558

  Leclere, P ^a   Ekstrom P ^b   Edstrom A ^b   Priestley, J ^c   Averill, S ^c   Tonge, D A ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b LUND UNIVERSITY   (Sweden)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Dorsal root ganglia; Mouse; Nerve regeneration; NGF; trk receptors

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; COLLAGEN TYPE 1; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; K 252A; MATRIGEL; NERVE GROWTH FACTOR; NEUROTROPHIN; NEUROTROPHIN RECEPTOR; PROTEIN KINASE INHIBITOR;

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LABELING; CONTROLLED STUDY; EXPLANT; MAMMAL; MOUSE; NERVE CELL CULTURE; NERVE CELL NECROSIS; NERVE FIBER GROWTH; NONHUMAN; PERIPHERAL NERVE; PRIORITY JOURNAL; SATELLITE CELL; SENSORY NERVE CELL; SPINAL GANGLION;

EID: 0342276126     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00307-2     Document Type: Article

References (58)

1. Aldskogius H., Wiesenfeld-Hallin Z., Kristensson K. Selective neuronal destruction by Ricinus communis agglutinin 1 and its use for the quantitative determination of sciatic nerve dorsal root ganglion cell numbers. Brain Res. 461:1988;215-220.
2. Averill S., McMahon S. B., Clary D. O., Reichardt L. F., Priestley J. V. Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur. J. Neurosci. 7:1995;1484-1494.
3. Barbacid M. Neurotrophic factors and their receptors. Curr. Opin. Cell Biol. 7:1995;148-155.
4. Baron R., Jänig W., McLachlan E. M. The afferent and efferent sympathetic components of the lumbar spinal outflow to the colon and pelvic organs in the cat. II. The lumbar splanchnic nerves. J. comp. Neurol. 238:1985;147-157.
5. Bennett D. L. H., Ramachandran N., Priestley J. V. and McMahon S. B. (1997), GDNF is a trophic factor for the neurotrophin independent population of adult sensory neurons (1996). Soc. Neurosci. Abstr. 23.
6. Bennett D. L. H., Averill S., Clary D. O., Priestley J. V., McMahon S. B. Post-natal changes in the expression of the trkA high affinity NGF receptor in primary sensory neurones. Eur. J. Neurosci. 8:1996;2204-2208.
7. Buj-Bello A., Buchman V. L., Horton A., Rosenthal A., Davis A. M. GDNF is an age-specific survival factor for sensory and autonomic neurons. Neuron. 15:1995;821-828.
8. Carbonetto S. The extracellular matrix of the nervous system. Trends Neurosci. 7:1994;382-387.
9. Choi-Lundberg D. L., Bohn M. C. Ontogeny and distribution of glial cell line-derived neurotrophic factor (GDNF) mRNA in rat. Devl Brain Res. 85:1995;80-88.
10. Durbec P., Marcos-Gutierrez C. V., Kilkenny C., Grigoriou M., Wartiowaara K., Suvanto P., Smith D., Ponder B., Constantini F., Saarma M., Sariola H., Pachnus V. GDNF signalling through the Ret receptor tyrosine kinase. Nature. 381:1996;789-793.
11. Ebendal T. (1989) Use of collagen gels to bioassay nerve growth factor activity. In Nerve Growth Factors (ed. Rush R.), pp. 81-93. John Wiley and Son Ltd.
12. Ebendal T., Tomac A., Hoffer B. J., Olsen L. Glial cell line-derived neurotrophic factor stimulates fibre formation and survival in cultured neurons from peripheral autonomic ganglia. J. Neurosci. Res. 40:1995;276-284.
13. 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. Neuroscience. 75:1996;1165-1174.
14. Ekström P. A. Neurons and glial cells of the mouse sciatic nerve undergo apoptosis after injury in vivo and in vitro. NeuroReport. 6:1995;1029-1032.
15. 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.
16. Gavrieli Y., Sherman Y., Ben-Sasson S. Identification of programmed cell death in situ via specific labelling of nuclear DNA fragmentation. J. Cell Biol. 119:1992;493-501.
17. Henderson C. E., Phillips H. S., Pollock R. A., Davies A. M., Lemeulle C., Armanini M., Simpson L. C., Moffat B., Vandlen R. A., Koliatsos V. E., Rosenthal A. GDNF: a potent survival for motoneurons present in peripheral nerve and muscle. Science. 266:1994;1062-1064.
18. Heumann R., Korsching S., Bandtlow C., Thoenen H. Changes of nerve growth factor synthesis in response to sciatic nerve transection. J. Cell Biol. 104:1987;1623-1631.
19. Honda C. Differential distribution of calbindin-D28k and parvalbumin in somatic and visceral sensory neurons. Neuroscience. 68:1995;883-892.
20. Hu-Tsai M., Winter J., Emson P. C., Woolf C. J. Neurite outgrowth and GAP 43 expression in cultured adult rat dorsal root ganglion neurons: effects of NGF or prior peripheral axotomy. J. Neurosci. Res. 39:1994;634-645.
21. Jiang Z.-G., Smith R. A., Neilson M. M. A. The effects of nerve growth factor on neurite outgrowth from cultured adult and aged mouse sensory neurons. Devl Brain Res. 85:1995;212-219.
22. 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.
23. Lawson S. N., Perry M. J., Prabhaker E., McCarthy P. W. Primary sensory neurons: neurofilament, neuropeptides and conduction velocity. Brain Res. Bull. 30:1993;239-243.
24. Li L., Wu W., Lin L.-F. H., Lei M., Oppenheim R. W., Houenou L. J. Rescue of adult motoneurons from injury-induced cell death by glial cell line-derived neurotrophic factor. Proc. natn. Acad. Sci. U.S.A. 92:1995;9771-9775.
25. Lin L.-F. H., Doherty D., Lile J., Bektesh S., Collins F. GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science. 260:1993;1130-1132.
26. Lindsay R. M. Nerve growth factors (NGF, BDNF) enhance axonal regeneration but are not required for survival of adult sensory neurons. J. Neurosci. 8:1988;2394-2408.
27. Lindsay R. M. (1992) The role of neurotrophic factors in functional maintenance of mature sensory neurons. In Sensory neurons. Development, Diversity and Plasticity, (ed. Scott S. A.), pp. 404-420. Oxford University Press, New York.
28. Malgrange B., Delree P., Rigo J. M., Baron H., Moonen G. Image analysis of neuritic regeneration by adult rat dorsal root ganglion neurons 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. Meth. 53:1994;111-122.
29. Matheson C. R., Carnahan J., Urich J. L., Bocangel D., Zhang T. J., Yan Q. Glail cell line-derived neurotrophic factor (GDNF) is a neurotrophic factor for sensory neurnons: Comparison of the effects to neurotrophins. J. Neurobiol. 32:1997;22-32.
30. 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.
31. McMahon S. B., Armanini M. P., Ling L. H., Phillips H. S. Expression and coexpression of trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron. 12:1994;1161-1171.
32. McMahon S. B., Priestley J. V. Peripheral neuropathies and neurotrophic factors: animal models and clinical perspectives. Curr. Opin. Neurosci. 5:1995;616-624.
33. Michael G. J., Klein R. D., Phillips H. S. and Priestley J. V. (1997), Expression of mRNAs for RET, GDNF-α and NTNR-α in identified rat lumbar DRG cell populations. Soc. Neurosci. Abstr. 23.
34. Mohiuddin L., Fernandez K., Tomlinson D. R., Fernyhough P. Nerve growth factor and neurotrophin-3 enhance neurite outgrowth and up-regulate the levels of messenger RNA for growth-associated protein GAP-43 and Tα1 α-tubulin in cultured adult rat sensory neurons. Neurosci. Lett. 185:1995;20-23.
35. Molliver D. C., Radeke M. J., Feinstein S. C., Snider W. D. Presence or absence of trkA protein distinguishes subsets of small sensory neurons with unique cytochemical characteristics and dorsal horn projections. J. comp. Neurol. 361:1995;404-416.
36. Moore M. W., Klein R. D., Fariñas I., Sauer H., Armanini M., Phillips H., Reichardt L. F., Ryan A. M., Carver-Moore K., Rosenthal A. Renal and neuronal abnormalities in mice lacking GDNF. Nature. 382:1996;76-79.
37. Muir D. Metalloprotease-dependent neurite outgrowth within a synthetic extracellular matrix is induced by nerve growth factor. Expl Cell Res. 210:1994;243-252.
38. Nicosia R. F., Ottinetti A. Growth of microvessels in serum-free matrix cultures of rat aorta. Lab. Invest. 63:1990;115-122.
39. Oppenheim R. W., Houenou L. J., Johnson J. E., Lin L.-P. H., Lo A. C., Newsome A. L., Prevette D. M., Wang S. Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF. Nature. 373:1995;344-346.
40. Peyronnard J.-M., Charron L. Motor and sensory neurons of the rat sural nerve: A horseradish peroxidase study. Muscle Nerve. 5:1982;654-660.
41. Peyronnard J.-M., Charron L., Messier J.-P., Lavoie J., Leger C., Faraco-Cantin F. Changes in lectin binding of lumbar dorsal root ganglia neurons and peripheral axons after sciatic and spinal nerve injury in the rat. Cell Tiss. Res. 257:1989;379-388.
42. Pichel J. G., Shen L., Sheng H. Z., Granholm A.-C., Drago J., Grinberg A., Lee E. J., Huang S. P., Saarma M., Hoffer B. J., Sariola H., Westphal H. Defects in enteric innervation and kidney development in mice lacking GDNF. Nature. 382:1996;73-76.
43. Raivich G., Kreutzberg G. W. Peripheral nerve regeneration: role of growth factors and their receptors. Int. J. dev. Neurosci. 3:1993;311-324.
44. Schaar D. G., Sieber B. A., Dreyfus C. F., Black I. B. Regional and cell-specific expression of GDNF in rat brain. Expl Neurol. 124:1993;368-371.
45. Sánchez M. P., Silos-Santiago I., Frisén J., He B., Lira S. A., Barbacid M. Renal agenisis and absence of enteric neurons in mice lacking GDNF. Nature. 382:1996;70-73.
46. Silos-Santiago I., Molliver D. C., Ozaki S., Smeyne R. J., Fagan A. M., Barbacid M., Snider W. D. Non-Trk A-expressing small DRG neurons are lost in Trk A deficient mice. J. Neurosci. 15:1995;5929-5942.
47. Snider W. G. Functions of the neurotrophins during nervous system development: what the knockouts are telling us. Cell. 77:1994;627-638.
48. Springer J. E., Seeberger J. L., He J., Gabres A., Blankenhorn E. P., Bergman L. W. cDNA sequence and differential mRNA regulation of two forms of glial cell line-derived neurotrophic factor in Schwann cells and rat skeletal muscle. Expl Neurol. 131:1995;47-52.
49. Strömberg I., Björklund L., Johansson M., Tomac A., Collins F., Olsen L., Hoffer B., Humpel C. Glial cell line-derived neurotrophic factor is expressed in the developing but not adult striatum and stimulates developing dopamine neurons in vivo. Expl Neurol. 124:1993;401-412.
50. 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.
51. 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.
52. 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. Neuroscience. 73:1996;541-551.
53. Treanor J. S., Goodman L., de Sauvage F., Stone D. M., Poulsen K. T., Beck C. D., Gray C., Armanini M. P., Pollock R. A., Hefti F., Phillips H. S., Goddard A., Moore M. W., Buj-Bello A., Davies A. M., Asai N., Takahashi M., Vandlen R., Henderson C. E., Rosenthal A. Characterization of a multicomponent receptor for GDNF. Nature. 382:1996;80-83.
54. 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.
55. 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.
56. Yan G., Matheson C., Lopes O. T. In vivo neurotrophic effects of GDNF on neonatal and adult facial motor neurons. Nature. 373:1995;341-344.
57. Ygge J. Neuronal loss in lumbar dorsal root ganglia after proximal compared to distal nerve resection: a quantitative study in the rat. Brain Res. 478:1989;193-195.
58. Zurn A. D., Baetge E. E., Hammang J. P., Tan S. A., Aebischer P. Glial cell line-derived factor (GDNF) a new neurotrophic factor for motoneurones. NeuroReport. 6:1994;113-118.