Competition for neurotrophic factor in the development of nerve connections

Proceedings of the Royal Society B: Biological Sciences

Volumn 266, Issue 1422, 1999, Pages 883-892

  Van Ooyen, Arjen ^a,b   Willshaw, David J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

Competition; Development of nerve connections; Neurodegeneration; Neurotrophic factors; Neurotrophin receptors; Regeneration

Indexed keywords

NEUROTROPHIC FACTOR; NEUROTROPHIN; NEUROTROPHIN RECEPTOR;

ARTICLE; INNERVATION; MODEL; NERVE DEGENERATION; NERVE FIBER GROWTH; NERVE GROWTH; NERVE REGENERATION; PRIORITY JOURNAL; SYNAPSE;

EID: 0033532140     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.1999.0719     Document Type: Article

References (49)

1. Albers, K. M., Wright, D. E. & Davies, B. M. 1994 Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system. J. Neurosci. 14, 1422-1432.
2. Barry, J. A. & Ribchester, R. R. 1995 Persistent polyneuronal innervation in partially denervated rat muscle after reinnervation and recovery from prolonged nerve conduction block. J. Neurosci. 15, 6327-6339.
3. Bennett, M. R. & Robinson, J. 1989 Growth and elimination of nerve terminals at synaptic sites during polyneuronal innervation of muscle cells: a trophic hypothesis. Proc. R. Soc. Lond. B 235, 299-320.
4. 125I-nerve growth factor with PC12 pheochromocytoma cells. Evidence for internalization via high affinity receptors only and for long-term regulation by nerve growth factor of both high-and low-affinity receptors. J. Biol. Chem. 259, 15509-15516.
5. LNGFR, in MAH cell. Science 257, 395-397.
6. Blöchel, A. & Thoenen, H. 1995 Characterization of nerve growth factor (NGF) release from hippocampal neurons: evidence for a constitutive and an unconventional sodium-dependent regulated pathway. Eur. J. Neurosci. 7, 1220-1228.
7. Bothwell, M. 1995 Functional interactions of neurotrophins and neurotrophin receptors. A. Rev. Neurosci. 18, 223-253.
8. Burgos, I., Cuello, A. C., Liberini, P., Pioro, E. & Masliah, E. 1995 NGF-mediated synaptic sprouting in the cerebral cortex of lesioned primate brain. Brain Res. 692, 154-160.
9. Cabelli, R. J., Hohn, A. & Shatz, C. J. 1995 Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science 267, 1662-1666.
10. Campenot, R. B. 1982 Development of sympathetic neurons in compartmentalized cultures. I. Local control of neurite growth by nerve growth factor. Dev. Biol. 93, 1-12.
11. Causing, C. G., Gloster, A., Aloyz, R., Bamji, S. X., Chang, E., Fawcett, J., Kuchel, G. & Miller, F. D. 1997 Synaptic innervation density is regulated by neuron-derived BDNF. Neuron 18, 257-267.
12. Cohen-Cory, S. & Fraser, S. E. 1995 Effects of brain-derived-neurotrophic factor on optic axon branching and remodelling in vivo. Nature 378, 192-196.
13. Cohen-Cory, S., Elliott, R. C., Dreyfus, C. F. & Black, I. B. 1993 Depolarizing influences increased low-affinity NGF receptor gene expression in cultured Purkinje neurons. Exp. Neurol. 119, 165-173.
14. Crepel, F. 1982 Regression of functional synapses in the immature mammalian cerebellum. Trends Neurosci. 5, 266-269.
15. Diamond, J., Holmes, M. & Coughlin, M. 1992 Endogenous NGF and nerve impulses regulate the collateral sprouting of sensory axons in the skin of the adult rat. J. Neurosci. 12, 1454-1466.
16. Edwards, R. H., Rutter, W. J. & Hanahan, D. 1989 Directed expression of NGF to pancreatic β cells in transgenic mice leads to selective hyperinnervation of the islets. Cell 58, 161-170.
17. Elliott, T. & Shadbolt, N. R. 1996 A mathematical model of activity-dependent, anatomical segregation induced by competition for neurotrophic support. Biol. Cybern. 75, 463-470.
18. ElShamy, W. M., Linnarsson, S., Lee, K.-F., Jaenisch, R. & Ernfors, P. 1996 Prenatal and postnatal requirements of NT-3 for sympathetic neuroblast survival and innervation of specific targets. Development 122, 491-500.
19. Funakoshi, H., Belluardo, N., Arenas, E., Yamamoto, Y., Casabona, A., Persson, H. & Ibáñez, C. F. 1995 Muscle-derived neurotrophin-4 as an activity-dependent trophic signal for adult motor neurons. Science 268, 1495-1499.
20. Garofalo, L., Ribeiro-da-Silva, A. & Cuello, C. 1992 Nerve growth factor-induced synaptogenesis and hypertrophy of cortical cholinergic terminals. Proc. Natl Acad. Sci. USA 89, 2639-2643.
21. Gouzé, J.-L., Lasry, J.-M. & Changeux, J.-P. 1983 Selective stabilization of muscle innervation during development: a mathematical model. Biol. Cybern. 46, 207-215.
22. Grinnell, A. D., Letinsky, M. S. & Rheuben, M. B. 1979 Competitive interaction between foreign nerves innervating frog skeletal muscle. J. Physiol. (Lond.) 289, 241-262.
23. trk mRNA marks NGF-responsive forebrain neurons: evidence that trk gene expression isinduced by NGF. Neuron 9, 465-478.
24. Hume, R. I. & Purves, D. 1981 Geometry of neonatal neurones and the regulation of synapse elimination. Nature 293, 469-471.
25. Jansen, J. K. S. & Fladby, T. 1990 The perinatal reorganization of the innervation of skeletal muscle in mammals. Prog. Neurobiol. 34, 39-90.
26. Jeanprêtre, N., Clarke, P. G. H. & Gabriel, J.-P. 1996 Competitive exclusion between axons dependent on a single trophic substance: a mathematical analysis. Math. Biosci. 133, 23-54.
27. Layer, P. G. & Shooter, E. M. 1983 Binding and degradation of nerve growth factor by PC12 pheochromocytoma cells. J. Biol. Chem. 258, 3012-3018.
28. Lewin, G. R. & Barde, Y.-A. 1996 Physiology of the neurotrophins. A. Rev. Neurosci. 19, 289-317.
29. Li, Y., Holtzman, D. M., Kromer, L. F., Kaplan, D. R., Chua-Couzens, J., Clary, D. O., Knüsel, B. & Mobley, W. C. 1995 Regulation of TrkA and ChAT expression in developing rat basal forebrain: evidence that both exogenous and endogenous NGF regulate differentiation of cholinergic neurons. J. Neurosci. 15, 2888-2905.
30. Lindsay, R. M., Shooter, E. M., Radeke, M. J., Misko, T. P., Dechant, G., Thoenen, H. & Lindholm, D. 1990 Nerve growth factor regulates expression of the nerve growth factor receptor gene in adult sensory neurons. Eur. J. Neurosci. 2, 389-396.
31. Miller, F. D., Speelman, A., Mathew, T. C., Fabian, J., Chang, E., Pozniak, C. & Toma, J. G. 1994 Nerve growth factor derived from terminals selectively increases the ratio of p75 to trkA NGF receptors on mature sympathetic neurons. Dev. Biol. 161, 260-217.
32. Ninkina, N., Adu, J., Fischer, A., Piñón, L. G. P., Buchman, V. L. & Davies, A. M. 1996 Expression and function of TrkB variants in developing sensory neurons. EMBO J. 15, 6385-6393.
33. Purves, D. 1988 Body and brain: a trophic theory of neural connections. Cambridge, MA: Harvard University Press.
34. Purves, D. & Lichtman, J. W. 1980 Elimination of synapses in the developing nervous system. Science 210, 153-157.
35. Purves, D. & Lichtman, J. W. 1985 Principles of neural development. Sunderland, MA: Sinauer.
36. Rasmussen, C. E. & Willshaw, D. J. 1993 Presynaptic and postsynaptic competition in models for the development of neuromuscular connections. Biol. Cybern. 68, 409-419.
37. Ribchester, R. R. 1988 Activity-dependent and -independent synaptic interactions during reinnervation of partially denervated rat muscle. J. Physiol. 401, 53-75.
38. Ribchester, R. R. & Barry, J. A. 1994 Spatial versus consumptive competition at polyneuronally innervated neuromuscular junctions. Exp. Physiol. 79, 465-494.
39. Rylett, R. J. & Williams, L. R. 1994 Role of neurotrophins in cholinergic-neurone function in the adult and aged CNS. Trends Neurosci. 17, 486-490.
40. Salehi, A., Verhaagen, J., Dijkhuizen, P. & Swaab, D. F. 1996 Co-localization of high-affinity neurotrophin receptors in nucleus basalis of meynert neurons and their differential reduction in Alzheimer's disease. Neuroscience 75, 373-387.
41. Schnell, L., Schneider, R., Kolbeck, R., Barde, Y.-A. & Schwab, M. E. 1994 Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 367, 170-173.
42. Sutter, A., Riopelle, R. J., Harris-Warrick, R. M. & Shooter, E. M. 1979 Nerve growth factor receptors. Characterization of two distinct classes of binding sites on chick embryo sensory ganglia cells. J. Biol. Chem. 254, 5972-5982.
43. Van Ooyen, A. & Willshaw, D. J. 1998 Poly-and mononeuronal innervation in a model for the development of neuromuscular connections. J. Theor. Biol. 196, 495-511.
44. Van Ooyen, A. & Willshaw, D. J. 1999 The development of nerve connections under neurotrophic control as a general consumer resource system. J. Theor. Biol. (Submitted.)
45. Wiley, H. S. & Cunningham, D. D. 1981 A steady state model for analyzing the cellular binding, internalization and degradation of polypeptide ligands. Cell 25, 433-440.
46. Yasuda, T., Sobue, G., Ito, T., Mitsuma, T. & Takahashi, A. 1990 Nerve growth factor enhances neurite arborization of adult sensory neurons; a study in single-cell culture. Brain Res. 524, 54-63.
47. Yodzis, P. 1989 Introduction to theoretical ecology. New York: Harper & Row.
48. Yunshao, H., Zhibin, Y., Yaoming, G., Guobi, K. & Yici, C. 1992 Nerve growth factor promotes collateral sprouting of cholinergic fibres in the septohippocampal cholinergic system of aged rats with fimbria transection. Brain Res. 586, 27-35.
49. Zupan, A. A. & Johnson, E. M. Jr 1991 Evidence for endocytosis-dependent proteolysis in the generation of soluble truncated nerve growth factor receptors by A875 human melanoma cells. J. Biol. Chem. 266, 15384-15390.