 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
Volume 16, Number 10, Issue of May 15, 1996 pp. 3256-3264
Copyright ©1996 Society for NeuroscienceSynaptic Modulation by Neurotrophic Factors: Differential and Synergistic Effects of Brain-Derived Neurotrophic Factor and Ciliary Neurotrophic Factor
Received Nov. 13, 1995; revised Feb. 26, 1996; accepted Feb. 28, 1996.
Ron Stoop and Mu-ming Poo Department of Biological Sciences, Columbia University, New York, New York 10027
Extracellular application of brain-derived neurotrophic factor (BDNF) and ciliary neurotrophic factor (CNTF) to developing neuromuscular junctions in Xenopus nerve-muscle cultures resulted in an increase in the frequency of spontaneous synaptic currents (SSCs) and in the amplitude of nerve-evoked synaptic currents. Analyses of the amplitude and time course of the SSCs suggest that these effects are attributable to elevation of presynaptic transmitter release. The actions of these two factors on the transmitter secretion process, however, are distinctly different. Fura-2 Ca2+ imaging showed that an increase in presynaptic cytosolic Ca2+ ([Ca2+]i) accompanied the synaptic potentiation by BDNF, whereas no change in [Ca2+]i was observed during synaptic potentiation by CNTF. Removing external Ca2+ also abolished the potentiating effect of BDNF but did not influence the CNTF effect. Moreover, the two factors exerted different effects on the short-term synaptic plasticity. Paired-pulse facilitation normally found at these synapses was reduced by BDNF but unaffected by CNTF; CNTF, but not BDNF, reduced the extent of synaptic depression during high-frequency tetanic stimulation. Finally, the potentiation effect of BDNF and CNTF on spontaneous transmitter release was additive when both factors were applied together to the synapse at saturating concentrations (100 ng/ml) and was highly synergistic when low doses (1 and 10 ng/ml) of both factors were used. These results suggest that because of their differential effects on the secretory machinery, BDNF and CNTF may act cooperatively in modulating the development and functioning of synapses.
Key words: BDNF; CNTF; neurotransmitter release; Fura-2 imaging; paired-pulse facilitation; synaptic plasticity; synergism
This article has been cited by other articles:
M. D. Amaral and L. Pozzo-Miller
BDNF Induces Calcium Elevations Associated With IBDNF, a Nonselective Cationic Current Mediated by TRPC Channels
J Neurophysiol, October 1, 2007; 98(4): 2476 - 2482.
[Abstract] [Full Text] [PDF]
G. Cao and C.-P. Ko
Schwann Cell-Derived Factors Modulate Synaptic Activities at Developing Neuromuscular Synapses
J. Neurosci., June 20, 2007; 27(25): 6712 - 6722.
[Abstract] [Full Text] [PDF]
W. J. Tyler, X.-l. Zhang, K. Hartman, J. Winterer, W. Muller, P. K. Stanton, and L. Pozzo-Miller
BDNF increases release probability and the size of a rapidly recycling vesicle pool within rat hippocampal excitatory synapses
J. Physiol., August 1, 2006; 574(3): 787 - 803.
[Abstract] [Full Text] [PDF]
C.-w. K. Wu and H. H. Yeh
Nerve Growth Factor Rapidly Increases Muscarinic Tone in Mouse Medial Septum/Diagonal Band of Broca
J. Neurosci., April 27, 2005; 25(17): 4232 - 4242.
[Abstract] [Full Text] [PDF]
A. P. Mizisin, Y. Vu, M. Shuff, and N. A. Calcutt
Ciliary Neurotrophic Factor Improves Nerve Conduction and Ameliorates Regeneration Deficits in Diabetic Rats
Diabetes, July 1, 2004; 53(7): 1807 - 1812.
[Abstract] [Full Text] [PDF]
X. Zhou, Q. Nai, M. Chen, J. D. Dittus, M. J. Howard, and J. F. Margiotta
Brain-Derived Neurotrophic Factor and trkB Signaling in Parasympathetic Neurons: Relevance to Regulating {alpha}7-Containing Nicotinic Receptors and Synaptic Function
J. Neurosci., May 5, 2004; 24(18): 4340 - 4350.
[Abstract] [Full Text] [PDF]
J. X. S. Jiang, R. C. Y. Choi, N. L. Siow, H. H. C. Lee, D. C. C. Wan, and K. W. K. Tsim
Muscle Induces Neuronal Expression of Acetylcholinesterase in Neuron-Muscle Co-culture: TRANSCRIPTIONAL REGULATION MEDIATED BY cAMP-DEPENDENT SIGNALING
J. Biol. Chem., November 14, 2003; 278(46): 45435 - 45444.
[Abstract] [Full Text] [PDF]
M. Neal, J. Cunningham, I. Lever, S. Pezet, and M. Malcangio
Mechanism by which Brain-Derived Neurotrophic Factor Increases Dopamine Release from the Rabbit Retina
Invest. Ophthalmol. Vis. Sci., February 1, 2003; 44(2): 791 - 798.
[Abstract] [Full Text] [PDF]
X.-P. He, L. Minichiello, R. Klein, and J. O. McNamara
Immunohistochemical Evidence of Seizure-Induced Activation of trkB Receptors in the Mossy Fiber Pathway of Adult Mouse Hippocampus
J. Neurosci., September 1, 2002; 22(17): 7502 - 7508.
[Abstract] [Full Text] [PDF]
M. Melis, R. Camarini, M. A. Ungless, and A. Bonci
Long-Lasting Potentiation of GABAergic Synapses in Dopamine Neurons after a Single In Vivo Ethanol Exposure
J. Neurosci., March 15, 2002; 22(6): 2074 - 2082.
[Abstract] [Full Text] [PDF]
C.-Y. Wang, F. Yang, X.-P. He, H.-S. Je, J.-Z. Zhou, K. Eckermann, D. Kawamura, L. Feng, L. Shen, and B. Lu
Regulation of Neuromuscular Synapse Development by Glial Cell Line-derived Neurotrophic Factor and Neurturin
J. Biol. Chem., March 15, 2002; 277(12): 10614 - 10625.
[Abstract] [Full Text] [PDF]
A. R. Carter, C. Chen, P. M. Schwartz, and R. A. Segal
Brain-Derived Neurotrophic Factor Modulates Cerebellar Plasticity and Synaptic Ultrastructure
J. Neurosci., February 15, 2002; 22(4): 1316 - 1327.
[Abstract] [Full Text] [PDF]
J. Xu, K. M. Gingras, L. Bengston, A. Di Marco, and N. G. Forger
Blockade of Endogenous Neurotrophic Factors Prevents the Androgenic Rescue of Rat Spinal Motoneurons
J. Neurosci., June 15, 2001; 21(12): 4366 - 4372.
[Abstract] [Full Text] [PDF]
D. S. Auld, F. Mennicken, and R. Quirion
Nerve Growth Factor Rapidly Induces Prolonged Acetylcholine Release from Cultured Basal Forebrain Neurons: Differentiation between Neuromodulatory and Neurotrophic Influences
J. Neurosci., May 15, 2001; 21(10): 3375 - 3382.
[Abstract] [Full Text] [PDF]
R. J. Kleiman, N. Tian, D. Krizaj, T. N. Hwang, D. R. Copenhagen, and L. F. Reichardt
BDNF-Induced Potentiation of Spontaneous Twitching in Innervated Myocytes Requires Calcium Release From Intracellular Stores
J Neurophysiol, July 1, 2000; 84(1): 472 - 483.
[Abstract] [Full Text] [PDF]
X.-p. He, F. Yang, Z.-p. Xie, and B. Lu
Intracellular Ca2+ and Ca2+/Calmodulin-dependent Kinase II Mediate Acute Potentiation of Neurotransmitter Release by Neurotrophin-3
J. Cell Biol., May 15, 2000; 149(4): 783 - 792.
[Abstract] [Full Text] [PDF]
M. M. Bolton, A. J. Pittman, and D. C. Lo
Brain-Derived Neurotrophic Factor Differentially Regulates Excitatory and Inhibitory Synaptic Transmission in Hippocampal Cultures
J. Neurosci., May 1, 2000; 20(9): 3221 - 3232.
[Abstract] [Full Text] [PDF]
T. Pizzorusso, G. M. Ratto, E. Putignano, and L. Maffei
Brain-Derived Neurotrophic Factor Causes cAMP Response Element-Binding Protein Phosphorylation in Absence of Calcium Increases in Slices and Cultured Neurons from Rat Visual Cortex
J. Neurosci., April 15, 2000; 20(8): 2809 - 2816.
[Abstract] [Full Text] [PDF]
M. Jia, M. Li, X.-W. Liu, H. Jiang, P. G. Nelson, and G. Guroff
Voltage-Sensitive Calcium Currents Are Acutely Increased by Nerve Growth Factor in PC12 Cells
J Neurophysiol, December 1, 1999; 82(6): 2847 - 2852.
[Abstract] [Full Text] [PDF]
T. Hamakawa, M. A. Woodin, M. C. Bjorgum, S. D. Painter, M. Takasaki, K. Lukowiak, G. T. Nagle, and N. I. Syed
Excitatory Synaptogenesis between Identified Lymnaea Neurons Requires Extrinsic Trophic Factors and Is Mediated by Receptor Tyrosine Kinases
J. Neurosci., November 1, 1999; 19(21): 9306 - 9312.
[Abstract] [Full Text] [PDF]
H. Jiang, K. Takeda, P. Lazarovici, Y. Katagiri, Z.-X. Yu, G. Dickens, A. Chabuk, X.-W. Liu, V. Ferrans, and G. Guroff
Nerve Growth Factor (NGF)-induced Calcium Influx and Intracellular Calcium Mobilization in 3T3 Cells Expressing NGF Receptors
J. Biol. Chem., September 10, 1999; 274(37): 26209 - 26216.
[Abstract] [Full Text] [PDF]
L. Boulanger and M. Poo
Gating of BDNF-Induced Synaptic Potentiation by cAMP
Science, June 18, 1999; 284(5422): 1982 - 1984.
[Abstract] [Full Text]
D. K. Binder, M. J. Routbort, and J. O. McNamara
Immunohistochemical Evidence of Seizure-Induced Activation of trk Receptors in the Mossy Fiber Pathway of Adult Rat Hippocampus
J. Neurosci., June 1, 1999; 19(11): 4616 - 4626.
[Abstract] [Full Text] [PDF]
B. S. Seebach, V. Arvanov, and L. M. Mendell
Effects of BDNF and NT-3 on Development of Ia/Motoneuron Functional Connectivity in Neonatal Rats
J Neurophysiol, May 1, 1999; 81(5): 2398 - 2405.
[Abstract] [Full Text] [PDF]
S. E. McKay, A. L. Purcell, and T. J. Carew
Regulation of Synaptic Function by Neurotrophic Factors in Vertebrates and Invertebrates: Implications for Development and Learning
Learn. Mem., May 1, 1999; 6(3): 193 - 215.
[Abstract] [Full Text]
W. A. Gottschalk, H. Jiang, N. Tartaglia, L. Feng, A. Figurov, and B. Lu
Signaling Mechanisms Mediating BDNF Modulation of Synaptic Plasticity in the Hippocampus
Learn. Mem., May 1, 1999; 6(3): 243 - 256.
[Abstract] [Full Text]
M. A. Woodin, T. Hamakawa, M. Takasaki, K. Lukowiak, and N. I. Syed
Trophic Factor-Induced Plasticity of Synaptic Connections Between Identified Lymnaea Neurons
Learn. Mem., May 1, 1999; 6(3): 307 - 316.
[Abstract] [Full Text]
S. Chang and S. V. Popov
Long-range signaling within growing neurites mediated by neurotrophin-3
PNAS, March 30, 1999; 96(7): 4095 - 4100.
[Abstract] [Full Text] [PDF]
S. Kinoshita, H. Yasuda, N. Taniguchi, R. Katoh-Semba, H. Hatanaka, and T. Tsumoto
Brain-Derived Neurotrophic Factor Prevents Low-Frequency Inputs from Inducing Long-Term Depression in the Developing Visual Cortex
J. Neurosci., March 15, 1999; 19(6): 2122 - 2130.
[Abstract] [Full Text] [PDF]
D. K. Binder, M. J. Routbort, T. E. Ryan, G. D. Yancopoulos, and J. O. McNamara
Selective Inhibition of Kindling Development by Intraventricular Administration of TrkB Receptor Body
J. Neurosci., February 15, 1999; 19(4): 1424 - 1436.
[Abstract] [Full Text] [PDF]
A. Shimada, C. A. Mason, and M. E. Morrison
TrkB Signaling Modulates Spine Density and Morphology Independent of Dendrite Structure in Cultured Neonatal Purkinje Cells
J. Neurosci., November 1, 1998; 18(21): 8559 - 8570.
[Abstract] [Full Text] [PDF]
C. Vicario-Abejon, C. Collin, R. D. G. McKay, and M. Segal
Neurotrophins Induce Formation of Functional Excitatory and Inhibitory Synapses between Cultured Hippocampal Neurons
J. Neurosci., September 15, 1998; 18(18): 7256 - 7271.
[Abstract] [Full Text] [PDF]
W. Gottschalk, L. D. Pozzo-Miller, A. Figurov, and B. Lu
Presynaptic Modulation of Synaptic Transmission and Plasticity by Brain-Derived Neurotrophic Factor in the Developing Hippocampus
J. Neurosci., September 1, 1998; 18(17): 6830 - 6839.
[Abstract] [Full Text] [PDF]
Q. Wang and J. Q. Zheng
cAMP-Mediated Regulation of Neurotrophin-Induced Collapse of Nerve Growth Cones
J. Neurosci., July 1, 1998; 18(13): 4973 - 4984.
[Abstract] [Full Text] [PDF]
E. N. Pothos, V. Davila, and D. Sulzer
Presynaptic Recording of Quanta from Midbrain Dopamine Neurons and Modulation of the Quantal Size
J. Neurosci., June 1, 1998; 18(11): 4106 - 4118.
[Abstract] [Full Text] [PDF]
M. E. Morrison and C. A. Mason
Granule Neuron Regulation of Purkinje Cell Development: Striking a Balance Between Neurotrophin and Glutamate Signaling
J. Neurosci., May 15, 1998; 18(10): 3563 - 3573.
[Abstract] [Full Text] [PDF]
M. D. Hilborn, R. R. Vaillancourt, and S. G. Rane
Growth Factor Receptor Tyrosine Kinases Acutely Regulate Neuronal Sodium Channels through the Src Signaling Pathway
J. Neurosci., January 15, 1998; 18(2): 590 - 600.
[Abstract] [Full Text] [PDF]
R. M. FITZSIMONDS and M.-M. POO
Retrograde Signaling in the Development and Modification of Synapses
Physiol Rev, January 1, 1998; 78(1): 143 - 170.
[Abstract] [Full Text] [PDF]
S. T. Lockhart, G. G. Turrigiano, and S. J. Birren
Nerve Growth Factor Modulates Synaptic Transmission between Sympathetic Neurons and Cardiac Myocytes
J. Neurosci., December 15, 1997; 17(24): 9573 - 9582.
[Abstract] [Full Text] [PDF]
M. Canossa, O. Griesbeck, B. Berninger, G. Campana, R. Kolbeck, and H. Thoenen
Neurotrophin release by neurotrophins: Implications for activity-dependent neuronal plasticity
PNAS, November 25, 1997; 94(24): 13279 - 13286.
[Abstract] [Full Text] [PDF]
Z.-P. Feng, J. Klumperman, K. Lukowiak, and N. I. Syed
In Vitro Synaptogenesis between the Somata of Identified Lymnaea Neurons Requires Protein Synthesis But Not Extrinsic Growth Factors or Substrate Adhesion Molecules
J. Neurosci., October 15, 1997; 17(20): 7839 - 7849.
[Abstract] [Full Text] [PDF]
G.-l. Ming, A. M. Lohof, and J. Q. Zheng
Acute Morphogenic and Chemotropic Effects of Neurotrophins on Cultured Embryonic Xenopus Spinal Neurons
J. Neurosci., October 15, 1997; 17(20): 7860 - 7871.
[Abstract] [Full Text] [PDF]
Y. Akaneya, T. Tsumoto, S. Kinoshita, and H. Hatanaka
Brain-Derived Neurotrophic Factor Enhances Long-Term Potentiation in Rat Visual Cortex
J. Neurosci., September 1, 1997; 17(17): 6707 - 6716.
[Abstract] [Full Text] [PDF]
M. A. Fahim
Endurance exercise modulates neuromuscular junction of C57BL/6NNia aging mice
J Appl Physiol, July 1, 1997; 83(1): 59 - 66.
[Abstract] [Full Text] [PDF]
K. Xie, T. Wang, P. Olafsson, K. Mizuno, and B. Lu
Activity-Dependent Expression of NT-3 in Muscle Cells in Culture: Implications in the Development of Neuromuscular Junctions
J. Neurosci., May 1, 1997; 17(9): 2947 - 2958.
[Abstract] [Full Text] [PDF]
H. Jiang, D. St. Ulme, G. Dickens, A. Chabuk, M. Lavarreda, P. Lazarovici, and G. Guroff
Both p140trk and p75NGFR Nerve Growth Factor Receptors Mediate Nerve Growth Factor-stimulated Calcium Uptake
J. Biol. Chem., March 14, 1997; 272(11): 6835 - 6837.
[Abstract] [Full Text] [PDF]
N. R. Holm, P. Christophersen, S. P. Olesen, and S. Gammeltoft
Activation of calcium-dependent potassium channels in rat brain neurons by neurotrophin-3 and nerve growth factor
PNAS, February 4, 1997; 94(3): 1002 - 1006.
[Abstract] [Full Text] [PDF]
H Kang, L Z Jia, K Y Suh, L Tang, and E M Schuman
Determinants of BDNF-induced hippocampal synaptic plasticity: role of the Trk B receptor and the kinetics of neurotrophin delivery.
Learn. Mem., January 1, 1996; 3(2-3): 188 - 196.
[Abstract] [PDF]
N. Tartaglia, J. Du, W. J. Tyler, E. Neale, L. Pozzo-Miller, and B. Lu
Protein Synthesis-dependent and -independent Regulation of Hippocampal Synapses by Brain-derived Neurotrophic Factor
J. Biol. Chem., September 28, 2001; 276(40): 37585 - 37593.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|