Involvement of Brain-Derived Neurotrophic Factor (BDNF) in the functional elimination of synaptic contacts at polyinnervated neuromuscular synapses during development

Journal of Neuroscience Research

Volumn 88, Issue 7, 2010, Pages 1406-1419

  Garcia, N ^a   Santafe, M M ^a   Tomas M ^a   Lanuza, M A ^a   Besalduch, N ^a   Tomas J ^a  

^a FACULTAT DE MEDICINA I CIÈNCIES DE LA SALUT   (Spain)

Author keywords

ACh release; Motor nerve terminals; Neuromuscular junction; p75NTR; Synapse elimination; tkB receptors

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CALCIUM CHANNEL L TYPE; CHOLINERGIC RECEPTOR STIMULATING AGENT; K 252A; NEUROTROPHIN; NEUROTROPHIN RECEPTOR P75; PROTEIN KINASE C;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL MATURATION; IMMUNOHISTOCHEMISTRY; MUSCLE CELL; NERVE ENDING; NEUROMUSCULAR SYNAPSE; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SCHWANN CELL; WESTERN BLOTTING;

ACETYLCHOLINE; ANIMALS; ANIMALS, NEWBORN; ANTIBODIES, BLOCKING; BRAIN-DERIVED NEUROTROPHIC FACTOR; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; NEURAL INHIBITION; NEUROMUSCULAR JUNCTION; NEURONAL PLASTICITY; PRESYNAPTIC TERMINALS; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, TRKB; RECEPTORS, NERVE GROWTH FACTOR; RECOMBINANT FUSION PROTEINS; SYNAPSES;

EID: 77952075403     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22320     Document Type: Article

References (49)

1. Alsina B, Vu T, Cohen-Cory S. 2001. Visualizing synapse formation in arborizing optic axons in vivo: dynamics and modulation by BDNF. Nat Neurosci 4:1093-1101. (Pubitemid 34116554)
2. Barde YA, Edgar D, Thoenen H. 1982. Purification of a new neurotrophic factor from mammalian brain. Embo J 1:549-553.
3. Blochl 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.
4. Boulanger LM, Poo MM. 1999. Presynaptic depolarization facilitates neurotrophin-induced synaptic potentiation. Nat Neurosci 2:346-351. (Pubitemid 30491277)
5. Frisen J, Verge VM, Fried K, Risling M, Persson H, Trotter J, Hokfelt T, Lindholm D. 1993. Characterization of glial trkB receptors: differential response to injury in the central and peripheral nervous systems. Proc Natl Acad Sci U S A 90:4971-4975. (Pubitemid 23182957)
6. Funakoshi H, Frisen J, Barbany G, Timmusk T, Zachrisson O, Verge VM, Persson H. 1993. Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve. J Cell Biol 123:455-465. (Pubitemid 23313968)
7. Funakoshi H, Belluardo N, Arenas E, Yamamoto Y, Casabona A, Persson H, Ibanez CF. 1995. Muscle-derived neurotrophin-4 as an activity-dependent trophic signal for adult motor neurons. Science 268:1495-1499.
8. Gall CM, Isackson PJ. 1989. Limbic seizures increase neuronal production of messenger RNA for nerve growth factor. Science 245:758-761.
9. Gonzalez M, Ruggiero FP, Chang Q, Shi YJ, Rich MM, Kraner S, Balice-Gordon RJ. 1999. Disruption of Trkb-mediated signaling induces disassembly of postsynaptic receptor clusters at neuromuscular junctions. Neuron 24:567-583.
10. Griesbeck O, Parsadanian AS, Sendtner M, Thoenen H. 1995. Expression of neurotrophins in skeletal muscle: quantitative comparison and significance for motoneuron survival and maintenance of function. J Neurosci Res 42:21-33.
11. Heumann R, Korsching S, Bandtlow C, Thoenen H. 1987. Changes of nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection. J Cell Biol 104:1623-1631. (Pubitemid 17104532)
12. Ip FC, Cheung J, Ip NY. 2001. The expression profiles of neurotrophins and their receptors in rat and chicken tissues during development. Neurosci Lett 301:107-110. (Pubitemid 32206697)
13. Jansen JK, Fladby T. 1990. The perinatal reorganization of the innervation of skeletal muscle in mammals. Prog Neurobiol 34:39-90. (Pubitemid 20052384)
14. Keller-Peck CR, Walsh MK, Gan WB, Feng G, Sanes JR, Lichtman JW. 2001. Asynchronous synapse elimination in neonatal motor units: studies using GFP transgenic mice. Neuron 31:381-394. (Pubitemid 32778558)
15. Koliatsos VE, Clatterbuck RE, Winslow JW, Cayouette MH, Price DL. 1993. Evidence that brain-derived neurotrophic factor is a trophic factor for motor neurons in vivo. Neuron 10:359-367.
16. Koliatsos VE, Cayouette MH, Berkemeier LR, Clatterbuck RE, Price DL, Rosenthal A. 1994. Neurotrophin 4/5 is a trophic factor for mammalian facial motor neurons. Proc Natl Acad Sci U S A 91:3304-3308. (Pubitemid 24130225)
17. Kwon YW, Gurney ME. 1996. Brain-derived neurotrophic factor transiently stabilizes silent synapses on developing neuromuscular junctions. J Neurobiol 29:503-516.
18. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
19. Lanuza MA, Garcia N, Santafe M, Nelson PG, Fenoll-Brunet MR, Tomas J. 2001. Pertussis toxin-sensitive G-protein and protein kinase C activity are involved in normal synapse elimination in the neonatal rat muscle. J Neurosci Res 63:330-340. (Pubitemid 32115280)
20. Loeb JA, Hmadcha A, Fischbach GD, Land SJ, Zakarian VL. 2002. Neuregulin expression at neuromuscular synapses is modulated by synaptic activity and neurotrophic factors. J Neurosci 22:2206-2214. (Pubitemid 35386520)
21. Lohof AM, Ip NY, Poo MM. 1993. Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature 363:350-353.
22. Mantilla CB, Zhan WZ, Sieck GC. 2004. Neurotrophins improve neuromuscular transmission in the adult rat diaphragm. Muscle Nerve 29:381-386.
23. McLachlan EM, Martin AR. 1981. Non-linear summation of end-plate potentials in the frog and mouse. J Physiol 311:307-324.
24. McKay SE, Garner A, Caldero J, Tucker RP, Large T, Oppenheim RW. 1996. The expression of trkB and p75 and the role of BDNF in the developing neuromuscular system of the chick embryo. Development 122:715-724. (Pubitemid 26054160)
25. Offenhauser N, Bohm-Matthaei R, Tsoulfas P, Parada L, Meyer M. 1995. Developmental regulation of full-length trkC in the rat sciatic nerve. Eur J Neurosci 7:917-925.
26. Oppenheim RW, Yin QW, Prevette D, Yan Q. 1992. Brain-derived neurotrophic factor rescues developing avian motoneurons from cell death. Nature 360:755-757. (Pubitemid 23012275)
27. Peng HB, Yang JF, Dai Z, Lee CW, Hung HW, Feng ZH, Ko CP. 2003. Differential effects of neurotrophins and schwann cell-derived signals on neuronal survival/growth and synaptogenesis. J Neurosci 23:5050-5060. (Pubitemid 36793232)
28. Pitts EV, Potluri S, Hess DM, Balice-Gordon RJ. 2006. Neurotrophin and Trk-mediated signaling in the neuromuscular system. Int Anesthesiol Clin 44:21-76. (Pubitemid 44507837)
29. Poo MM. 2001. Neurotrophins as synaptic modulators. Nat Rev Neurosci 2:24-32.
30. Pousinha PA, Diogenes MJ, Ribeiro JA, Sebastiao AM. 2006. Triggering of BDNF facilitatory action on neuromuscular transmission by adenosine A2A receptors. Neurosci Lett 404:143-147.
31. Redfern PA. 1970. Neuromuscular transmission in new-born rats. J Physiol 209:701-709.
32. Ribchester RR, Barry JA. 1994. Spatial versus consumptive competition at polyneuronally innervated neuromuscular junctions. Exp Physiol 79:465-494.
33. Roux S, Saint Cloment C, Curie T, Girard E, Mena FJ, Barbier J, Osta R, Molgo J, Brulet P. 2006. Brain-derived neurotrophic factor facilitates in vivo internalization of tetanus neurotoxin C-terminal fragment fusion proteins in mature mouse motor nerve terminals. Eur J Neurosci 24:1546-1554. (Pubitemid 44427523)
34. Sanes JR, Lichtman JW. 1999. Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22:389-442.
35. Santafe MM, Garcia N, Lanuza MA, Uchitel OD, Tomas J. 2001. Calcium channels coupled to neurotransmitter release at dually innervated neuromuscular junctions in the newborn rat. Neuroscience 102:697-708. (Pubitemid 32171888)
36. Santafe MM, Garcia N, Lanuza MA, Uchitel OD, Salon I, Tomas J. 2002. Decreased calcium influx into the neonatal rat motor nerve terminals can recruit additional neuromuscular junctions during the synapse elimination period. Neuroscience 110:147-154. (Pubitemid 34214766)
37. Santafe MM, Salon I, Garcia N, Lanuza MA, Uchitel OD, Tomas J. 2003. Modulation of ACh release by presynaptic muscarinic autoreceptors in the neuromuscular junction of the newborn and adult rat. Eur J Neurosci 17:119-127. (Pubitemid 36098882)
38. Santafe MM, Salon I, Garcia N, Lanuza MA, Uchitel OD, Thomas J. 2004. Muscarinic auto receptors related with calcium channels in the strong and weak inputs at polyinnervated developing rat neuromuscular junctions. Neuroscience 123:61-73. (Pubitemid 37518476)
39. Santafe MM, Garcia N, Lanuza MA, Tomas J. 2007. Protein kinase C activity affects neurotransmitter release at polyinnervated neuromuscular synapses. J Neurosci Res 85:1449-1457. (Pubitemid 46724388)
40. Santafe MM, Garcia N, Lanuza MA, Tomas M, Besalduch N, Tomas J. 2009. Presynaptic muscarinic receptors, calcium channels, and protein kinase C modulate the functional disconnection of weak inputs at polyinnervated neonatal neuromuscular synapses. J Neurosci Res 87:1195-1206.
41. Schecterson LC, Bothwell M. 1992. Novel roles for neurotrophins are suggested by BDNF and NT-3 mRNA expression in developing neurons. Neuron 9:449-463.
42. Sheard PW, Musaad K, Duxson MJ. 2002. Distribution of neurotrophin receptors in the mouse neuromuscular system. Int J Dev Biol 46:569-575. (Pubitemid 36841026)
43. Stoop R, Poo MM. 1996. Synaptic modulation by neurotrophic factors: differential and synergistic effects of brain-derived neurotrophic factor and ciliary neurotrophic factor. J Neurosci 16:3256-3264. (Pubitemid 26142359)
44. Todd KJ, Auld DS, Robitaille R. 2007. Neurotrophins modulate neuron-glia interactions at a vertebrate synapse. Eur J Neurosci 25:1287-1296. (Pubitemid 46568757)
45. Wang T, Xie K, Lu B. 1995. Neurotrophins promote maturation of developing neuromuscular synapses. J Neurosci 15:4796-4805.
46. Wang XH, Poo MM. 1997. Potentiation of developing synapses by postsynaptic release of neurotrophin-4. Neuron 19:825-835. (Pubitemid 27471387)
47. Yan Q, Johnson EM Jr. 1988. An immunohistochemical study of the nerve growth factor receptor in developing rats. J Neurosci 8:3481-3498.
48. Yang F, Je HS, Ji Y, Nagappan G, Hempstead B, Lu B. 2009. Pro-BDNF-induced synaptic depression and retraction at developing neuromuscular synapses. J Cell Biol 185:727-741.
49. Zhang Y, Moheban DB, Conway BR, Bhattacharyya A, Segal RA. 2000. Cell surface Trk receptors mediate NGF-induced survival while internalized receptors regulate NGF-induced differentiation. J Neurosci 20:5671-5678. (Pubitemid 30636894)