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Neurotrophins improve synaptic transmission in the adult rodent diaphragm

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Neurophysiology Aims and scope

Abstract

Neurotrophins are usually viewed as secreted proteins that control long-term survival and differentiation of neurons. However, recent studies have established that among the most important functions of neurotrophins is their capacity to regulate synaptic functions and plasticity. When altering synaptic function, neurotrophins are able to produce two types of outcomes, an immediate effect on synaptic transmission and long-term control of synaptic structure and function. The first effect occurs within seconds or minutes after the neurotrophic factor has been applied and usually involves acute modification of synaptic transmission. The second effect takes hours and days, as protein synthesis is required to complete the structural changes. Neurotrophins and their receptors are expressed within the neuromuscular system, making these agents ideal candidates for the short-and long-term regulation of skeletal muscle function. For instance, neurotrophins can alter neuromuscular function acutely, by modulating the amount of neurotransmitter released with each nerve impulse, or chronically, by changing postsynaptic properties or the content and size of synaptic vesicles. It is obvious that the effects of neurotrophins depend on the specific neurotrophin involved (four neurotrophins have been found in mammals; these are nerve growth factor, brain-derived neurotrophic factor, and neurotrophins-3 and-4) and on the specific synapse being studied. Growing evidence highlights the role of neurotrophins in the development and function of neuromuscular synapses. This review will examine the role of neurotrophins in the regulation of neuromuscular transmission.

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References

  1. S. Cohen, R. Levi-Montalcini, and V. Hamburger, “A nerve growth-stimulating factor isolated from sarcomas 37 and 180,” Proc. Natl. Acad. Sci. USA, 40, No. 10, 1014–1018 (1954).

    Article  PubMed  CAS  Google Scholar 

  2. G. Chevrel, R. Hohlfeld, and M. Sendtner, “The role of neurotrophins in muscle under physiological and pathological conditions,” Muscle Nerve, 33, No. 4, 462–476 (2006).

    Article  PubMed  CAS  Google Scholar 

  3. T. Timmusk, N. Belluardo, M. Metsis, and H. Persson, “Widespread and developmentally regulated expression of neurotrophin-4 messenger RNA in rat brain and peripheral tissues,” Eur. J. Neurosci., 5, No. 6, 605–613 (1993).

    Article  PubMed  CAS  Google Scholar 

  4. J. T. Erickson, J. C. Conover, V. Borday, et al., “Mice lacking brain-derived neurotrophic factor exhibit visceral sensory neuron losses distinct from mice lacking NT4 and display a severe developmental deficit in control of breathing,” J. Neurosci., 16, No. 17, 5361–5371 (1996).

    PubMed  CAS  Google Scholar 

  5. K. Seidl, C. Erck, and A. Buchberger, “Evidence for the participation of nerve growth factor and its low-affinity receptor (p75NTR) in the regulation of the myogenic program,” J. Cell Physiol., 176, No. 1, 10–21 (1998).

    Article  PubMed  CAS  Google Scholar 

  6. J. Widenfalk, K. Lundstromer, M. Jubran, et al., “Neurotrophic factors and receptors in the immature and adult spinal cord after mechanical injury or kainic acid,” J. Neurosci., 21, No. 10, 3457–3475 (2001).

    PubMed  CAS  Google Scholar 

  7. B. Lu, “BDNF and activity-dependent synaptic modulation,” Learn. Memory, 10, No. 2, 86–98 (2003).

    Article  Google Scholar 

  8. K. W. Kafitz, C. R. Rose, H. Thoenen, and A. Konnerth, “Neurotrophin-evoked rapid excitation through TrkB receptors,” Nature, 401, No. 6756, 918–921 (1999).

    Article  PubMed  CAS  Google Scholar 

  9. H. Kang and E. M. Schuman, “Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus,” Science, 267, No. 5204, 1658–1662 (1995).

    Article  PubMed  CAS  Google Scholar 

  10. A. F. Schinder and M. Poo, “The neurotrophin hypothesis for synaptic plasticity,” Trends Neurosci., 23, No. 12, 639–645 (2000).

    Article  PubMed  CAS  Google Scholar 

  11. M. M. Poo, “Neurotrophins as synaptic modulators,” Nat. Rev. Neurosci., 2, No. 1, 24–32 (2001).

    Article  PubMed  CAS  Google Scholar 

  12. R. E. Burke, “Motor units: anatomy, physiology and functional organization,” in: Handbook of Physiology. The Nervous System. Motor Control, Vol. 3, L. D. Peachey (ed.), Am. Physiol. Soc., Bethesda, MD (1981), pp. 345–422.

    Google Scholar 

  13. G. C. Sieck, M. Fournier, and J. G. Enad, “Fiber type composition of muscle units in the cat diaphragm,” Neurosci. Lett., 97, Nos. 1/2, 29–34 (1989).

    Article  PubMed  CAS  Google Scholar 

  14. J. Rettig and E. Neher, “Emerging roles of presynaptic proteins in Ca2+-triggered exocytosis,” Science, 298, No. 5594, 781–785 (2002).

    Article  PubMed  CAS  Google Scholar 

  15. R. B. Sutton, D. Fasshauer, R. Jahn, and A. T. Brunger, “Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution,” Nature, 395, No. 6700, 347–353 (1998).

    Article  PubMed  CAS  Google Scholar 

  16. Y. Dunant and M. Israel, “Neurotransmitter release at rapid synapses,” Biochimie, 82, No. 4, 289–302 (2000).

    Article  PubMed  CAS  Google Scholar 

  17. S. Sugita, O. H. Shin, W. Han, et al., “Synaptotagmins form a hierarchy of exocytotic Ca2+ sensors with distinct Ca2+ affinities,” EMBO J., 21, No. 3, 270–280 (2002).

    Article  PubMed  CAS  Google Scholar 

  18. C. Rosenmund, A. Sigler, I. Augustin, et al., “Differential control of vesicle priming and short-term plasticity by Munc13 isoforms,” Neuron, 33, No. 3, 411–424 (2002).

    Article  PubMed  CAS  Google Scholar 

  19. D. A. Richards, C. Guatimosim, S. O. Rizzoli, and W. J. Betz, “Synaptic vesicle pools at the frog neuromuscular junction,” Neuron, 39, No. 3, 529–541 (2003).

    Article  PubMed  CAS  Google Scholar 

  20. S. O. Rizzoli and W. J. Betz, “The structural organization of the readily releasable pool of synaptic vesicles,” Science, 303, No. 5666, 2037–2039 (2004).

    Article  PubMed  CAS  Google Scholar 

  21. C. B. Mantilla, K. L. Rowley, M. A. Fahim, et al., “Synaptic vesicle cycling at type-identified diaphragm neuromuscular junctions,” Muscle Nerve, 30, No. 6, 774–783 (2004).

    Article  PubMed  Google Scholar 

  22. L. G. Ermilov, C. B. Mantilla, K. L. Rowley, and G. C. Sieck, “Safety factor for neuromuscular transmission at type-identified diaphragm fibers,” Muscle Nerve, 35, No. 6, 800–803 (2007).

    Article  PubMed  Google Scholar 

  23. C. Rosenmund and C. F. Stevens, “Definition of the readily releasable pool of vesicles at hippocampal synapses,” Neuron, 16, No. 6, 1197–1207 (1996).

    Article  PubMed  CAS  Google Scholar 

  24. R. S. Zucker and W. G. Regehr, “Short-term synaptic plasticity,” Annu. Rev. Physiol., 64, 355–405 (2002).

    Article  PubMed  CAS  Google Scholar 

  25. T. C. Sudhof, “The synaptic vesicle cycle,” Annu. Rev. Neurosci., 27, 509–547 (2004).

    Article  PubMed  CAS  Google Scholar 

  26. M. H. Ellisman, J. E. Rash, L. A. Staehelin, and K. R. Porter, “Studies of excitable membranes. II. A comparison of specializations at neuromuscular junctions and nonjunctional sarcolemmas of mammalian fast and slow twitch muscle fibers,” J. Cell Biol., 68, No. 3, 752–774 (1976).

    Article  PubMed  CAS  Google Scholar 

  27. D. F. Wilson, “Depression, facilitation, and mobilization of transmitter at the rat diaphragm neuromuscular junction,” Am. J. Physiol., 237, No. 1, C31–C37 (1979).

    PubMed  CAS  Google Scholar 

  28. V. A. Pieribone, O. Shupliakov, L. Brodin, et al., “Distinct pools of synaptic vesicles in neurotransmitter release,” Nature, 375, No. 6531, 493–497 (1995).

    Article  PubMed  CAS  Google Scholar 

  29. B. Reid, C. R. Slater, and G. S. Bewick, “Synaptic vesicle dynamics in rat fast and slow motor nerve terminals,” J. Neurosci., 19, No. 7, 2511–2521 (1999).

    PubMed  CAS  Google Scholar 

  30. J. del Castillo and B. Katz, “Quantal components of the end-plate potential,” J. Physiol., 124, No. 3, 560–573 (1954).

    Google Scholar 

  31. B. Katz and S. Thesleff, “On the factors which determine the amplitude of the ‘miniature end-plate potential’,” J. Physiol., 137, No. 2, 267–278 (1957).

    PubMed  CAS  Google Scholar 

  32. M. I. Glavinovic, “Change of statistical parameters of transmitter release during various kinetic tests in unparalysed voltage-clamped rat diaphragm,” J. Physiol., 290, No. 2, 481–497 (1979).

    PubMed  CAS  Google Scholar 

  33. D. Elmqvist and D. M. Quastel, “A quantitative study of end-plate potentials in isolated human muscle,” J. Physiol., 178, No. 3, 505–529 (1965).

    PubMed  CAS  Google Scholar 

  34. W. J. Betz, “Depression of transmitter release at the neuromuscular junction of the frog,” J. Physiol., 206, No. 3, 629–644 (1970).

    PubMed  CAS  Google Scholar 

  35. B. N. Christensen and A. R. Martin, “Estimates of probability of transmitter release at the mammalian neuromuscular junction,” J. Physiol., 210, No. 4, 933–945 (1970).

    PubMed  CAS  Google Scholar 

  36. R. E. Burke, D. N. Levine, and F. E. Zajac, 3rd, “Mammalian motor units: physiological-histochemical correlation in three types in cat gastrocnemius,” Science, 174, No. 10, 709–712 (1971).

    Article  PubMed  CAS  Google Scholar 

  37. R. E. Burke, D. N. Levine, P. Tsairis, and F. E. Zajac, 3rd, “Physiological types and histochemical profiles in motor units of the cat gastrocnemius,” J. Physiol., 234, No. 3, 723–748 (1973).

    PubMed  CAS  Google Scholar 

  38. M. Fournier and G. C. Sieck, “Mechanical properties of muscle units in the cat diaphragm,” J. Neurophysiol., 59, No. 3, 1055–1066 (1988).

    PubMed  CAS  Google Scholar 

  39. M. H. Brooke and K. K. Kaiser, “Muscle fiber types: how many and what kind?” Arch. Neurol., 23, No. 4, 369–379 (1970).

    PubMed  CAS  Google Scholar 

  40. G. C. Sieck, R. R. Roy, P. Powell, et al., “Muscle fiber type distribution and architecture of the cat diaphragm,” J. Appl. Physiol., 55, No. 5, 1386–1392 (1983).

    PubMed  CAS  Google Scholar 

  41. S. Schiaffino and C. Reggiani, “Myosin isoforms in mammalian skeletal muscle,” J. Appl. Physiol., 77, No. 2, 493–501 (1994).

    PubMed  CAS  Google Scholar 

  42. G. C. Sieck, W. Z. Zhan, Y. S. Prakash, et al., “SDH and actomyosin ATPase activities of different fiber types in rat diaphragm muscle,” J. Appl. Physiol., 79, No. 5, 1629–1639 (1995).

    PubMed  CAS  Google Scholar 

  43. S. Schiaffino and C. Reggiani, “Molecular diversity of myofibrillar proteins: Gene regulation and functional significance,” Physiol. Rev., 76, 371–423 (1996).

    PubMed  CAS  Google Scholar 

  44. D. Pette and R. S. Staron, “Myosin isoforms, muscle fiber types, and transitions,” Microsc. Res. Tech., 50, No. 6, 500–509 (2000).

    Article  PubMed  CAS  Google Scholar 

  45. P. M. Nemeth, L. Solanki, D. A. Gordon, et al., “Uniformity of metabolic enzymes within individual motor units,” J. Neurosci., 6, No. 3, 892–898 (1986).

    PubMed  CAS  Google Scholar 

  46. G. C. Sieck, M. Fournier, Y. S. Prakash, and C. E. Blanco, “Myosin phenotype and SDH enzyme variability among motor unit fibers,” J. Appl. Physiol., 80, No. 6, 2179–2189 (1996).

    PubMed  CAS  Google Scholar 

  47. H. P. Clamann and A. J. Robinson, “A comparison of electromyographic and mechanical fatigue properties in motor units of the cat hindlimb,” Brain Res., 327, Nos. 1/2, 203–219 (1985).

    PubMed  CAS  Google Scholar 

  48. G. C. Sieck and M. Fournier, “Changes in diaphragm motor unit EMG during fatigue,” J. Appl. Physiol., 68, No. 5, 1917–1926 (1990).

    PubMed  CAS  Google Scholar 

  49. Y. S. Prakash, S. M. Miller, M. Huang, and G. C. Sieck, “Morphology of diaphragm neuromuscular junctions on different fibre types,” J. Neurocytol., 25, No. 2, 88–100 (1996).

    Article  PubMed  CAS  Google Scholar 

  50. G. C. Sieck and Y. S. Prakash, “Morphological adaptations of neuromuscular junctions depend on fiber type,” Can. J. Appl. Physiol., 22, No. 3, 197–230 (1997).

    PubMed  CAS  Google Scholar 

  51. Y. S. Prakash, M. J. Cody, P. R. Housmans, et al., “Comparison of cross-bridge cycling kinetics in neonatal vs. adult rat ventricular muscle,” J. Muscle Res. Cell Motil., 20, No. 7, 717–723 (1999).

    Article  PubMed  CAS  Google Scholar 

  52. M. A. Fahim, J. A. Holley, and N. Robbins, “Topographic comparison of neuromuscular junctions in mouse slow and fast twitch muscles,” Neuroscience, 13, No. 1, 227–235 (1984).

    Article  PubMed  CAS  Google Scholar 

  53. B. D. Johnson and G. C. Sieck, “Differential susceptibility of diaphragm muscle fibers to neuromuscular transmission failure,” J. Appl. Physiol., 75, No. 1, 341–348 (1993).

    PubMed  CAS  Google Scholar 

  54. T. E. Dick, F. J. Kong, and A. J. Berger, “Correlation of recruitment order with axonal conduction velocity for supraspinally driven diaphragmatic motor units,” J. Neurophysiol., 57, No. 1, 245–259 (1987).

    PubMed  CAS  Google Scholar 

  55. G. C. Sieck and M. Fournier, “Diaphragm motor unit recruitment during ventilatory and nonventilatory behaviors,” J. Appl. Physiol., 66, No. 6, 2539–2545 (1989).

    PubMed  CAS  Google Scholar 

  56. C. B. Mantilla, K. L. Rowley, W. Z. Zhan, et al., “Synaptic vesicle pools at diaphragm neuromuscular junctions vary with motoneuron soma, not axon terminal, inactivity,” Neuroscience, 146, No. 1, 178–189 (2007).

    Article  PubMed  CAS  Google Scholar 

  57. D. Pette and R. S. Staron, “Cellular and molecular diversities of mammalian skeletal muscle fibers,” Rev. Physiol. Biochem. Pharmacol., 116, 1–76 (1990).

    PubMed  CAS  Google Scholar 

  58. S. J. Wood and C. R. Slater, “The contribution of postsynaptic folds to the safety factor for neuromuscular transmission in rat fast-and slow-twitch muscles,” J. Physiol., 500, No. 1, 165–176 (1997).

    PubMed  CAS  Google Scholar 

  59. B. Reid, V. N. Martinov, A. Nja, et al., “Activity-dependent plasticity of transmitter release from nerve terminals in rat fast and slow muscles,” J. Neurosci., 23, No. 28, 9340–9348 (2003).

    PubMed  CAS  Google Scholar 

  60. E. G. T. Liddell and C. S. Sherrington, “Recruitment and some other factors of reflex inhibition,” Proc. Roy. Soc. London, Ser. Biol., 97, 488–518 (1925).

    Article  Google Scholar 

  61. C. S. Sherrington, “Some functional problems attaching to convergence,” Proc. Roy. Soc. London, Ser. Biol., 105, 332–362 (1929).

    Google Scholar 

  62. E. Henneman, “Relation between size of neurons and their susceptibility to discharge,” Science, 126, No. 3287, 1345–1346 (1957).

    Article  PubMed  CAS  Google Scholar 

  63. E. Henneman, G. Somjen, and D. O. Carpenter, “Functional significance of cell size in spinal motoneurons,” J. Neurophysiol., 28, No. 3, 560–580 (1965).

    PubMed  CAS  Google Scholar 

  64. J. S. Jodkowski, F. Viana, T. E. Dick, and A. J. Berger, “Electrical properties of phrenic motoneurons in the cat: correlation with inspiratory drive,” J. Neurophysiol., 58, No. 1, 105–124 (1987).

    PubMed  CAS  Google Scholar 

  65. J. W. Fleshman, J. B. Munson, G. W. Sypert, and W. A. Friedman, “Rheobase, input resistance, and motor-unit type in medial gastrocnemius motoneurons in the cat,” J. Neurophysiol., 46, No. 6, 1326–1338 (1981).

    PubMed  CAS  Google Scholar 

  66. G. W. Sypert and J. B. Munson, “Basis of segmental motor control: Motoneuron size or motor unit type?” Neurosurgery, 8, No. 5, 608–621 (1981).

    Article  PubMed  CAS  Google Scholar 

  67. D. G. Stuart and R. M. Enoka, “Motoneurons, motor units, and the size principle.” in: The Clinical Neurosciences, R. N. Rosenberg (ed.), Churchill Livingstone, New York (1983), pp. 471–517.

    Google Scholar 

  68. B. Walmsley, J. A. Hodgson, and R. E. Burke, “Forces produced by medial gastrocnemius and soleus muscles during locomotion in freely moving cats,” J. Neurophysiol., 41, No. 5, 1203–1216 (1978).

    PubMed  CAS  Google Scholar 

  69. G. C. Sieck, “Recruitment and frequency coding of diaphragm motor units during ventilatory and non-ventilatory behaviors.” in: Respiratory Control, G. D. Swanson, F. S. Grodins, and R. L. Hughson (eds.), Plenum Press, New York (1989), pp. 441–450.

    Google Scholar 

  70. G. C. Sieck, “Neural control of the inspiratory pump,” NIPS, 6, 260–264 (1991).

    Google Scholar 

  71. G. C. Sieck and Y. S. Prakash, “The diaphragm muscle.” in: Neural Control of the Respitatory Muscles, A. D. Miller, A. L. Bianchi, and B. P. Bishop (eds.), CRC Press, Boca Raton, FL (1997), pp. 7–20.

    Google Scholar 

  72. J. B. Harris and R. R. Ribchester, “The relationship between end-plate size and transmitter release in normal and dystrophic muscles of the mouse,” J. Physiol., 296, 245–265 (1979).

    PubMed  CAS  Google Scholar 

  73. S. S. Kelly and N. Robbins, “Progression of age changes in synaptic transmission at mouse neuromuscular junctions,” J. Physiol., 343, 375–383 (1983).

    PubMed  CAS  Google Scholar 

  74. A. G. Engel, “The neuromuscular junction,” in: Myology: Basic and Clinical, A. G. Engel, and C. Franzini Armstrong (eds.), McGraw-Hill, New York (1994), pp. 261–302.

    Google Scholar 

  75. S. J. Wood and C. R. Slater, “Safety factor at the neuromuscular junction,” Prog. Neurobiol., 64, No. 4, 393–429 (2001).

    Article  PubMed  CAS  Google Scholar 

  76. R. A. Gertler and N. Robbins, “Differences in neuromuscular transmission in red and white muscles,” Brain Res., 142, No. 1, 160–164 (1978).

    Article  PubMed  CAS  Google Scholar 

  77. C. C. Chang, S. T. Chuang, and M. C. Huang, “Effects of chronic treatment with various neuromuscular blocking agents on the number and distribution of acetylcholine receptors in the rat diaphragm,” J. Physiol., 250, No. 1, 161–173 (1975).

    PubMed  CAS  Google Scholar 

  78. S. S. Kelly, “The effect of age on neuromuscular transmission,” J. Physiol., 274, 51–62 (1978).

    PubMed  CAS  Google Scholar 

  79. A. C. Wareham, R. H. Morton, and G. H. Meakin, “Low quantal content of the endplate potential reduces safety factor for neuromuscular transmission in the diaphragm of the newborn rat,” Br. J. Anaesth., 72, No. 2, 205–209 (1994).

    Article  PubMed  CAS  Google Scholar 

  80. M. S. Biring, M. Fournier, D. J. Ross, and M. I. Lewis, “Cellular adaptations of skeletal muscles to cyclosporine,” J. Appl. Physiol., 84, No. 6, 1967–1975 (1998).

    PubMed  CAS  Google Scholar 

  81. R. J. Talmadge, “Myosin heavy chain isoform expression following reduced neuromuscular activity: potential regulatory mechanisms,” Muscle Nerve, 23, No. 5, 661–679 (2000).

    Article  PubMed  CAS  Google Scholar 

  82. Y. A. Barde, “Trophic factors and neuronal survival,” Neuron, 2, No. 6, 1525–1534 (1989).

    Article  PubMed  CAS  Google Scholar 

  83. A. M. Davies, “Neurobiology. Tracking neurotrophin function,” Nature, 368, No. 6468, 193–194 (1994).

    Article  PubMed  CAS  Google Scholar 

  84. H. Thoenen, “Neurotrophins and neuronal plasticity,” Science, 270, No. 5236, 593–598 (1995).

    Article  PubMed  CAS  Google Scholar 

  85. M. Barbacid, “The Trk family of neurotrophin receptors,” J. Neurobiol., 25, No. 11, 1386–1403 (1994).

    Article  PubMed  CAS  Google Scholar 

  86. D. R. Kaplan and F. D. Miller, “Neurotrophin signal transduction in the nervous system,” Curr. Opin. Neurobiol., 10, No. 3, 381–391 (2000).

    Article  PubMed  CAS  Google Scholar 

  87. E. J. Huang and L. F. Reichardt, “Neurotrophins: roles in neuronal development and function,” Annu. Rev. Neurosci., 24, 677–736 (2001).

    Article  PubMed  CAS  Google Scholar 

  88. H. Funakoshi, J. Frisen, G. Barbany, et al., “Differential expression of mRNAs for neurotrophins and their receptors after axotomy,” J. Cell Biol., 123, 455–465 (1993).

    Article  PubMed  CAS  Google Scholar 

  89. O. Griesbeck, A. S. Parsadanian, M. Sendtner, and H. Thoenen, “Expression of neurotrophins in skeletal muscle: quantitative comparison and significance for motoneuron survival and maintenance of function,” J. Neurosci. Res., 42, No. 1, 21–33 (1995).

    Article  PubMed  CAS  Google Scholar 

  90. F. C. Ip, J. Cheung, and N. Y. Ip, “The expression profiles of neurotrophins and their receptors in rat and chicken tissues during development,” Neurosci. Lett., 301, No. 2, 107–110 (2001).

    Article  PubMed  CAS  Google Scholar 

  91. D. M. Hess, M. O. Scott, S. Potluri, et al., “Localization of TrkC to Schwann cells and effects of neurotrophin-3 signaling at neuromuscular synapses,” J. Comp. Neurol., 501, No. 4, 465–482 (2007).

    Article  PubMed  CAS  Google Scholar 

  92. L. C. Schecterson and M. Bothwell, “Novel roles for neurotrophins are suggested by BDNF and NT-3 mRNA expression in developing neurons,” Neuron, 9, No. 3, 449–463 (1992).

    Article  PubMed  CAS  Google Scholar 

  93. C. E. Henderson, W. Camu, C. Mettling, et al., “Neurotrophins promote motor neuron survival and are present in embryonic limb bud,” Nature, 363, 266–270 (1993).

    Article  PubMed  CAS  Google Scholar 

  94. V. E. Koliatsos, R. E. Clatterbuck, J. W. Winslow, et al., “Evidence that brain-derived neurotrophic factor is a trophic factor for motor neurons in vivo,” Neuron, 10, No. 3, 359–367 (1993).

    Article  PubMed  CAS  Google Scholar 

  95. R. A. Johnson, A. J. Okragly, M. Haak-Frendscho, and G. S. Mitchell, “Cervical dorsal rhizotomy increases brain-derived neurotrophic factor and neurotrophin-3 expression in the ventral spinal cord,” J. Neurosci., 20, No. 10, RC 77 (2000).

    Google Scholar 

  96. P. W. Sheard, K. Musaad, and M. J. Duxson, “Distribution of neurotrophin receptors in the mouse neuromuscular system,” Int. J. Dev. Biol., 46, No. 4, 569–575. (2002).

    PubMed  CAS  Google Scholar 

  97. M. Gonzalez, F. P. Ruggiero, Q. Chang, et al., “Disruption of Trkb-mediated signaling induces disassembly of postsynaptic receptor clusters at neuromuscular junctions,” Neuron, 24, No. 3, 567–583 (1999).

    Article  PubMed  CAS  Google Scholar 

  98. W. Z. Zhan, C. B. Mantilla, and G. C. Sieck, “Regulation of neuromuscular transmission by neurotrophins,” Sheng Li Xue Bao, 55, No. 6, 617–624 (2003).

    PubMed  CAS  Google Scholar 

  99. Y. Kovalchuk, K. Holthoff, and A. Konnerth, “Neurotrophin action on a rapid timescale,” Curr. Opin. Neurobiol., 14, No. 5, 558–563 (2004).

    Article  PubMed  CAS  Google Scholar 

  100. C. B. Mantilla, W. Z. Zhan, and G. C. Sieck, “Neurotrophins improve neuromuscular transmission in the adult rat diaphragm,” Muscle Nerve, 29, No. 3, 381–386 (2004).

    Article  PubMed  CAS  Google Scholar 

  101. A. M. Lohof, N. Y. Ip, and M. M. Poo, “Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF,” Nature, 363, No. 6427, 350–353 (1993).

    Article  PubMed  CAS  Google Scholar 

  102. X. H. Wang, and M. M. Poo, “Potentiation of developing synapses by postsynaptic release of neurotrophin-4,” Neuron, 19, No. 4, 825–835 (1997).

    Article  PubMed  CAS  Google Scholar 

  103. L. Boulanger and M. M. Poo, “Presynaptic depolarization facilitates neurotrophin-induced synaptic potentiation,” Nat. Neurosci., 2, No. 4, 346–351 (1999).

    Article  PubMed  CAS  Google Scholar 

  104. R. J. Kleiman, N. Tian, D. Krizaj, et al., “BDNF-induced potentiation of spontaneous twitching in innervated myocytes requires calcium release from intracellular stores,” J. Neurophysiol., 84, No. 1, 472–483 (2000).

    PubMed  CAS  Google Scholar 

  105. V. N. Kaliunov, L. G. Ermilov, and S. V. Shmalei, “Effect of nerve growth factor on synaptic processes in the sympathetic ganglion,” Sechenov Fiziol. Zh. SSSR, 74, No. 1, 49–56 (1988).

    CAS  Google Scholar 

  106. V. N. Kaliunov, L. G. Ermilov, and S. V. Shmalei, “The function of the cholinoreactive systems of the postsynaptic neuron under the action of nerve growth factor,” Nerv. Sistemy, 27, 41–48 (1988).

    CAS  Google Scholar 

  107. K. Xie, T. Wang, P. Olafsson, et al., “Activity-dependent expression of NT-3 in muscle cells in culture: implications in the development of neuromuscular junctions,” J. Neurosci., 17, No. 9, 2947–2958. (1997).

    PubMed  CAS  Google Scholar 

  108. S. S. Zakharenko, S. L. Patterson, I. Dragatsis, et al., “Presynaptic BDNF required for a presynaptic but not postsynaptic component of LTP at hippocampal CA1-CA3 synapses,” Neuron, 39, No. 6, 975–990 (2003).

    Article  PubMed  CAS  Google Scholar 

  109. H. Funakoshi, N. Belluardo, E. Arenasa, et al., “Muscle-derived neurotrophin-4 as an activity-dependent trophic signal for adult motor neurons,” Science, 268, 1495–1499 (1995).

    Article  PubMed  CAS  Google Scholar 

  110. K. Sakuma, K. Watanabe, M. Sano, et al., “A possible role for BDNF, NT-4 and TrkB in the spinal cord and muscle of rat subjected to mechanical overload, bupivacaine injection and axotomy,” Brain Res., 907, Nos. 1/2, 1–19 (2001).

    Article  PubMed  CAS  Google Scholar 

  111. S. Copray and D. Kernell, “Neurotrophins and trk-receptors in adult rat spinal motoneurons: differences related to cell size but not to ’slow/fast’ specialization,” Neurosci. Lett., 289, No. 3, 217–220 (2000).

    Article  PubMed  CAS  Google Scholar 

  112. K. Kimpinski, R. B. Campenot, and K. Mearow, “Effects of the neurotrophins nerve growth factor, neurotrophin-3, and brain-derived neurotrophic factor (BDNF) on neurite growth from adult sensory neurons in compartmented cultures,” J. Neurobiol., 33, No. 4, 395–410 (1997).

    Article  PubMed  CAS  Google Scholar 

  113. J. A. Loeb, A. Hmadcha, G. D. Fischbach, et al., “Neuregulin expression at neuromuscular synapses is modulated by synaptic activity and neurotrophic factors,” J. Neurosci., 22, No. 6, 2206–2214. (2002).

    PubMed  CAS  Google Scholar 

  114. L. M. Moscoso, G. C. Chu, M. Gautam, et al., “Synapse-associated expression of an acetylcholine receptor-inducing protein, ARIA/heregulin, and its putative receptors, ErbB2 and ErbB3, in developing mammalian muscle,” Dev. Biol., 172, No. 1, 158–169 (1995).

    Article  PubMed  CAS  Google Scholar 

  115. N. Altiok, S. Altiok, and J. P. Changeux, “Heregulin-stimulated acetylcholine receptor gene expression in muscle: requirement for MAP kinase and evidence for a parallel inhibitory pathway independent of electrical activity,” EMBO J., 16, No. 4, 717–725 (1997).

    Article  PubMed  CAS  Google Scholar 

  116. A. W. Sandrock, Jr., S. E. Dryer, K. M. Rosen, et al., “Maintenance of acetylcholine receptor number by neuregulins at the neuromuscular junction in vivo,” Science, 276, No. 5312, 599–603 (1997).

    Article  PubMed  Google Scholar 

  117. N. Belluardo, H. Westerblad, G. Mudo, et al., “Neuromuscular junction disassembly and muscle fatigue in mice lacking neurotrophin-4,” Mol. Cell Neurosci., 18, No. 1, 56–67 (2001).

    Article  PubMed  CAS  Google Scholar 

  118. D. G. Wells, B. A. McKechnie, S. Kelkar, and J. R. Fallon, “Neurotrophins regulate agrin-induced postsynaptic differentiation,” Proc. Natl. Acad. Sci. USA, 96, No. 3, 1112–1117 (1999).

    Article  PubMed  CAS  Google Scholar 

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Correspondence to G. C. Sieck.

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Neirofiziologiya/Neurophysiology, Vol. 39, Nos. 4/5, pp. 327–337, July–October, 2007.

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Ermilov, L.G., Sieck, G.C., Zhan, Wz. et al. Neurotrophins improve synaptic transmission in the adult rodent diaphragm. Neurophysiology 39, 284–293 (2007). https://doi.org/10.1007/s11062-007-0039-0

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