Synergistic but transient rescue effects of BDNF and GDNF on axotomized neonatal motoneurons

Neuroscience

Volumn 84, Issue 1, 1998, Pages 129-139

  Vejsada, R ^a   Tseng, J L ^b   Lindsay, R M ^c   Acheson, A ^c   Aebischer, P ^b   Kato, A C ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^c REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

Axotomy; Cell death; Continuous administration; Motoneuron; Neurotrophic factors

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DEATH; MODEL; MOTONEURON; NERVE FIBER TRANSECTION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SCIATIC NERVE;

ANIMALS; ANIMALS, NEWBORN; AXOTOMY; BRAIN-DERIVED NEUROTROPHIC FACTOR; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG COMBINATIONS; DRUG SYNERGISM; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; MOTOR NEURONS; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 0031938822     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00497-1     Document Type: Article

References (57)

1. Acheson A., Conover J. C., Fandl J. P., DeChiara T. M., Russell M., Thadani A., Squinto S. P., Yancopoulos G. D., Lindsay R. M. A BDNF autocrine loop in adult sensory neurons prevents cell death. Nature. 374:1995;450-453.
2. Aebischer P., Pochon N. A.-M., Heyd B., Déglon N., Joseph J.-M., Zurn A., Baetge E. E., Hammang J. P., Goddard M., Lysaght M., Kaplan F., Kato A. C., Schluep M., Hirt L., Regli F., Porchet F., de Tribolet N. Gene therapy for Amyotrophic Lateral Sclerosis (ALS) using a polymer encapsulated xenogenic cell line engineered to secrete hCNTF. Hum. Gen. Ther. 7:1996;851-860.
3. Anderson K. D., Panayotatos N., Corcoran T. L., Lindsay R. M., Wiegand S. J. Ciliary neurotrophic factor protects striatal output neurons in an animal model of Huntington disease. Proc. natn. Acad. Sci. U.S.A. 93:1996;7346-7351.
4. Arakawa Y., Sendtner M., Thoenen H. Survival effect of ciliary neurotrophic factor (CNTF) on chick embryonic motoneurons in culture: comparison with other neurotrophic factors and cytokines. J. Neurosci. 10:1990;3507-3515.
5. Buchman V. L., Davies A. M. Different neurotrophins are expressed and act in a developmental sequence to promote the survival of embryonic sensory neurons. Development. 118:1993;989-1001.
6. ω-nitro-L-arginine methyl ester of motoneuron cell death after neonatal axotomy. Neuroscience. 71:1996;313-325.
7. Cheema S. S., Richards L. J., Murphy M., Bartlett P. F. Leukaemia inhibitory factor rescues motoneurones from axotomy-induced cell death. NeuroReport. 5:1994;989-992.
8. DeBilbao F., Dubois-Dauphin M. Time course of axotomy-induced apoptotic cell death in facial motoneurons of neonatal wild type and bcl-2 transgenic mice. Neuroscience. 71:1996;1111-1119.
9. Efron B. Bootstrap methods: another look at the jack-knife. Ann. Statist. 7:1979;1-26.
10. Eriksson N. P., Lindsay R. M., Aldskogius H. BDNF and NT-3 rescue sensory but not motoneurones following axotomy in the neonate. NeuroReport. 5:1994;1445-1448.
11. Finiels F., Gimenez y Ribota M., Barkats M., Samolyk M.-L., Robert J.-J., Privat A., Revah F., Mallet J. Specific and efficient gene transfer strategy offers new potentialities for the treatment of motor neurone diseases. NeuroReport. 7:1995;373-378.
12. Frank L., Ventimiglia R., Anderson K., Lindsay R. M., Rudge J. S. BDNF down-regulates neurotrophin responsiveness, TrkB protein and TrkB mRNA levels in cultured rat hippocampal neurons. Eur. J. Neurosci. 8:1996;1220-1230.
13. Friedman B., Kleinfeld D., Ip N. Y., Verge V. M. K., Moulton R., Boland P., Zlotchenko E., Lindsay R. M., Liu L. BDNF and NT-4/5 exert neurotrophic influences on injured adult spinal motor neurons. J. Neurosci. 15:1995;1044-1056.
14. Greensmith L., Mentis G., Vrbová G. Blockade of N-methyl-D-aspartate receptors by MK-801 (dizocilpine maleate) rescues motoneurons in developing rats. Devl Brain Res. 81:1994;162-170.
15. Greensmith L., Dick J., Emanuel A. O., Vrbová G. Induction of transmitter release at the neuromuscular junction prevents motoneuron death after axotomy in neonatal rats. Neuroscience. 71:1996;213-220.
16. Hayes V., Cadelli D., Kato A. C. Differential modulation of the cholinergic activity of rat CNS neurons in culture. Devl Brain Res. 62:1991;159-168.
17. Henderson C. E. (1995) Neurotrophic factors as therapeutic agents in amyotrophic lateral sclerosis. Potential and pitfalls. In Pathogenesis and Therapy of Amyotrophic Latral Sclerosis (eds Serratrice G. and Munsat T.), Advances in Neurology, Vol. 68, pp. 235-240. Lippincott-Raven, Philadelphia.
18. Henderson C. E., Phillips H. S., Pollock R. A., Davies A. M., Lemeulle C., Armanini M., Simpson L. C., Moffet B., Vandlen R. A., Koliatsos V. E., Rosenthal A. GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science. 266:1994;1062-1064.
19. Hoffman D., Wahlberg L., Aebischer P. NGF released from a polymer matrix prevents loss of ChAT expression in basal forebrain neurons following a fimbria-fornix lesion. Expl Neurol. 110:1990;39-44.
20. Hoffman D., Breakefield X. O., Short M. P., Aebischer P. Transplantation of a polymer-encapsulated cell line genetically engineered to release NGF. Expl Neurol. 122:1993;100-106.
21. Houenou L. J., Oppenheim R.W. Motoneuron death during development, following injury and in neurological disease. Semin. Neurosci. 6:1994;283-289.
22. Hughes R. A., Sendtner M., Thoenen H. Members of several gene families influence survival of rat motoneurons in vitro and in vivo. J. Neurosci. Res. 36:1993;663-671.
23. Iwasaki Y., Shiojima T., Tagaya N., Kobayashi T., Kinoshita M. Effect of transforming growth factor β1 on spinal motor neurons after axotomy. J. neurol. Sci. 147:1997;9-12.
24. Kato A. C., Lindsay R. M. Overlapping and additive effects of neurotrophins and CNTF on cultured human spinal cord neurons. Expl Neurol. 130:1994;196-201.
25. Koliatsos V. E., Cayouette M. H., Berkemeier L. R., Clatterbuck R. E., Price D. L., Rosenthal A. Neurotrophin 4/5 is a trophic factor for mammalian facial motor neurons. Proc. natn. Acad. Sci. U.S.A. 91:1994;3304-3308.
26. Kordower J.H., Winn S.R., Liu Y.-T., Musfon E.J., Slade J.R., Hammang J.P., Baetge E.E., Emerich D.F. The aged monkey basal forebrain: rescue and sprouting of axotomized basal forebrain neurons after grafts of encapsulated cells secreting human nerve growth factor. Proc. natn. Acad. Sci. U.S.A. 91:1994;10898-10902.
27. Li L., Oppenheim R. W., Lei M., Houenou L. J. Neurotrophic agents prevent motoneuron death following sciatic nerve section in the neonatal mouse. J. Neurobiol. 25:1994;759-766.
28. Li L., Wu W., Lin L.-F. H., 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. natn. Acad. Sci. U.S.A. 92:1995;9771-9775.
29. Lin L.-F. H., Doherty D. H., Lile J. D., Bektesh S., Collins F. GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science. 260:1993;1130-1132.
30. Lindsay R., Thoenen H., Barde Y.-A. Placode and neural crest-derived sensory neurons are responsive at early developmental stages to brain-derived neurotrophic factor (BDNF). Devl Biol. 112:1985;319-328.
31. Lowrie G., Vrbová G. Dependence of postnatal motoneurones on their targets: review and hypothesis. Trends Neurosci. 15:1992;80-84.
32. Martinou J.-C., Martinou I., Kato A. C. Cholinergic differentiation factor promotes survival of rat embryonic motoneurons in vitro. Neuron. 8:1992;737-744.
33. Matheson C. R., Wang J., Collins F. D., Yan Q. Long-term survival effects of GDNF on neonatal rat facial motoneurons after axotomy. NeuroReport. 8:1997;1739-1742.
34. Mitsumoto H., Ikeda K., Klinkosz B., Cedarbaum J. M., Wong V., Lindsay R. M. Arrest of motor neuron disease in wobbler mice cotreated with CNTF and BDNF. Science. 265:1994;1107-1110.
35. 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. 200:1995;45-48.
36. Oppenheim R. W., Prevette D., McKay S., Cardwell C. Motoneuron survival in vivo after treatment with combinations of muscle- and CNS-derived trophic factors. Soc. Neurosci. Abstr. 19:1993;416.
37. Oppenheim R. W., Prevette D., Haverkamp L. J., Houenou L., Yin Q.-W., McManaman J. Biological studies of a putative avian muscle-derived neurotrophic factor that prevents naturally occurring motoneuron death in vivo. J. Neurobiol. 241:1993;1065-1079.
38. Oppenheim R. W., Houenou L. J., Johnson J. E., Lin L.-F. H., Li L., 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.
39. Oppenheim R. W. Neurotrophic survival molecules for motoneurons: an embarrassment of riches. Neuron. 17:1996;195-197.
40. Pennica D., Arce V., Swanson T. A., Vejsada R., Pollock R. A., Armanini M., Dudley K., Phillips H. S., Rosenthal A., Kato A. C., Henderson C. E. Cardiotrophin-1, a cytokine present in embryonic muscle, supports long-term survival of a sub-population of motoneurons. Neuron. 17:1996;1-20.
41. Sagot Y., Tan S. A., Baetge E., Schmalbruch H., Kato A. C., Aebischer P. Polymer encapsulated cell lines genetically engineered to release ciliary neurotrophic factor can slow down progressive motor neuronopathy in the mouse. Eur. J. Neurosci. 7:1995;1313-1322.
42. Sagot Y., Tan S. A., Hammang J., Aebischer P., Kato A. C. GDNF slows loss of motoneurons but not axonal degeneration or premature death of pmn/pmn mice. J. Neurosci. 16:1996;2335-2341.
43. Schmalbruch H., Rosenthal A. Neurotrophin-4/5 postpones the death of injured spinal motoneurons in newborn rats. Brain Res. 700:1995;254-260.
44. Sendtner M., Holtmann R., Kolbeck R., Thoenen H., Barde Y.-A. Brain-derived neurotrophic factor prevents the death of motoneurons in newborn rats after nerve section. Nature. 360:1992;757-759.
45. Sendtner M., Schmalbruch H., Stöckli K. A., Carroll P., Kreutzberg G. W., Thoenen H. Ciliary neurotrophic factor prevents degeneration of motor neurons in mouse mutant progressive motor neuronopathy. Nature. 358:1992;502-504.
46. Sendtner M., Kreutzberg G. W., Thoenen H. Ciliary neurotrophic factor prevents the degeneration of motor neurons after axotomy. Nature. 345:1990;440-441.
47. Snider W. D., Elliot J. L., Yan Q. Axotomy-induced neuronal death during development. J. Neurobiol. 23:1992;1231-1246.
48. Tseng J. L., Baetge E. E., Zurn A. D., Aebischer P. GDNF reduces drug-induced rotational behavior after medial forebrain bundle transection by a mechanism not involving striatal dopamine. J. Neurosci. 17:1996;325-333.
49. Tuszynski M.H., Mafong E., Meyer S. Central infusions of brain-derived neurotrophic factor and neurotrophin-4/5, but not nerve growth factor and neurotrophin-3, prevent loss of the cholinergic phenotype in injured adult motor neurons. Neuroscience. 71:1996;761-771.
50. Vejsada R., Sagot Y., Kato A. C. BDNF-mediated rescue of axotomized motoneurons decreases with increasing dose. NeuroReport. 5:1994;1889-1892.
51. Vejsada R., Sagot Y., Kato A. C. Quantitative comparison of the transient rescue effects of neurotrophic factors on axotomized motoneurons in vivo. Eur. J. Neurosci. 7:1995;108-115.
52. Wong V., Arriaga R., Ip N. Y., Lindsay R. M. The neurotrophins BDNF, NT-3, and NT-4/5, but not NGF, up-regulate the cholinergic phenotype of developing motor neurons. Eur. J. Neurosci. 5:1993;466-474.
53. Yan Q., Elliott J. L., Snider W. D. Brain-derived neurotrophic factor rescues spinal motor neurons from axotomy-induced cell death. Nature. 360:1992;753-755.
54. Yan Q., Matheson C., Lopez O. T., Miller J. A. The biological responses of axotomized adult motoneurons to brain-derived neurotrophic factor. J. Neurosci. 14:1994;5281-5291.
55. Yan Q., Matheson C., Lopez O. T. In vivo neurotrophic effects of GDNF on neonatal and adult facial motor neurons. Nature. 373:1995;341-344.
56. Zurn A. D., Baetge E. E., Hammang J. P., Tan S. A., Aebischer P. Glial cell line-derived neurotrophic factor (GDNF), a new neurotrophic factor for motoneurones. NeuroReport. 6:1994;113-118.
57. Zurn A. D., Winkel L., Menoud A., Djabali K., Aebischer P. Combined effects of GDNF, BDNF, and CNTF on motoneuron differentiation in vitro. J. Neurosci. Res.