Autogenic modulation of mechanoreceptor excitability by glutamate release from synaptic-like vesicles: Evidence from the rat muscle spindle primary sensory ending

Journal of Physiology

Volumn 562, Issue 2, 2005, Pages 381-394

  Bewick, Guy S ^a   Reid, Brian ^a   Richardson, Christine ^b   Banks, Robert W ^b  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b DURHAM UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

3,5 DIHYDROXYPHENYLGLYCINE; CALCIUM ION; DYE; GLUTAMIC ACID; IONOTROPIC RECEPTOR ANTAGONIST; KYNURENIC ACID; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR ANTAGONIST; PHOSPHOLIPASE D; CALCIUM; IONOTROPIC RECEPTOR;

AFFERENT NERVE GROUP 1; AMINO ACID TRANSPORT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; IMMUNOGOLD ELECTRON MICROSCOPY; MALE; MECHANICAL STIMULATION; MECHANORECEPTOR; MECHANOTRANSDUCTION; MUSCLE EXCITATION; MUSCLE SPINDLE; MUSCLE STRETCHING; NERVE ENDING; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE VESICLE; ADULT; ELECTRON MICROSCOPY; EXCITABILITY; IMMUNOGOLD LABELING; SYNAPTIC LIKE VESICLE;

ANIMALS; CALCIUM; COBALT; CYCLOPROPANES; ELECTROPHYSIOLOGY; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; FLUORESCENT DYES; GLUTAMIC ACID; GLYCINE; IMMUNOHISTOCHEMISTRY; MALE; MECHANORECEPTORS; MEMBRANE POTENTIALS; MICROSCOPY, FLUORESCENCE; MUSCLE SPINDLES; NERVE ENDINGS; NEURONS, AFFERENT; PATCH-CLAMP TECHNIQUES; RATS; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPTIC VESICLES;

EID: 12744277989     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2004.074799     Document Type: Article

References (53)

1. Adal MN (1969). The fine structure of the sensory region of cat muscle spindles. J Ultrastruct Res 26, 332-354.
2. Aguado F, Majó G, Ruiz-Montasell B, Llorens J, Marsal J & Blasi J (1999). Syntaxin 1A and 1B display distinct distribution patterns in the rat peripheral nervous system. Neuroscience 88, 437-446.
3. Akoev GN, Alekseev NP & Krylov BV (1988). Mechanoreceptors: Their Functional Organization. Springer-Verlag, Berlin.
4. Albani-Torregrossa S, Attucci S, Marinozzi M, Pellicciari R, Moroni F & PellegriniGiampietro DE (1999). Antagonist pharmacology of metabotropic glutamate receptors coupled to phospholipase D activation in adult rat hippocampus: focus on (2R,1′S,2′ R,3′ S)-2-(2′-carboxy-3′ -phenylcyclopropyl) glycine versus 3,5-dihydroxyphenylglycine. Mol Pharmacol 55, 699-707.
5. Banks RW, Bewick GS, Reid B & Richardson AC (2002). Evidence for activity-dependent modulation of sensory-terminal excitability in spindles by glutamate release from synaptic-like vesicles. Adv Exp Med Biol 508, 13-18.
6. Banks RW, Richardson C & Bewick GS (2000). Immunocytochemical demonstration of glutamate in the sensory terminals of rat muscle spindles. J Physiol 528.P, 62P.
7. Betz WJ & Bewick GS (1992). Optical analysis of synaptic vesicle recycling at the frog neuromuscular junction. Science 255, 200-203.
8. Betz WJ, Mao F & Bewick GS (1992). Activity-dependent fluorescent staining and destaining of living vertebrate motor nerve terminals. J Neurosci 12, 363-375.
9. Bewick GS, Duncan R, Eddie W, Maguire C & Banks RW (2004). Glutamate-enhanced muscle spindle excitability - inhibition by PLD-coupled metabotropic glutamate receptor antagonists. J Physiol 557.P, 65P.
10. Bewick GS, Reid B & Banks RW (2000). Investigating the role of small clear vesicles in vertebrate mechanosensory endings using rat muscle spindles. J Physiol 528.P, 62-63P.
11. Cauna N (1966). Fine structure of the receptor organs and its probable functional significance. In Touch, Heat and Pain, ed. De Reuck AVS & Knight J, pp. 117-136. Churchill, London.
12. Chua M & Hunt CC (1995). Sensory endings of living isolated mammalian muscle spindles. In Alpha and Gamma Motor Systems, ed. Taylor A, Gladden MH & Durbaba R, pp. 251-254. Plenum Press, New York.
13. Cochilla AJ, Angelson JK & Betz WJ (1999). Monitoring secretory membrane with FM1-43 fluorescence. Annu Rev Neurosci 22, 1-10.
14. Conradi S, Cullheim S, Gollvik L & Kellerth J-O (1983). Electron microscopic observations on the synaptic contacts of group Ia muscle spindle afferents in the cat lumbosacral spinal cord. Brain Res 265, 31-39.
15. Dale HH (1935). Pharmacology and nerve endings. Proc R Soc Med 28, 319-332.
16. De Camilli P, Vitadello M, Canevini MP, Zanoni R, Jahn R & Gorio A (1988). The synaptic vesicle proteins synapsin-I and synaptophysin (protein-p38) are concentrated both in efferent and afferent nerve-endings of the skeletal-muscle. J Neurosci 8, 1625-1631.
17. De-Doncker L, Picquet F, Petit J & Falempin M (2003). Characterization of spindle afferents in rat soleus muscle using ramp-and-hold and sinusoidal stretches. J Neurophysiol 89, 442-449.
18. Dow PR, Shinn SL & Ovalle WK (1980). Ultrastructural study of a blood-muscle spindle barrier after systemic administration of horseradish peroxidase. Am J Anat 157, 375-388.
19. Duc C, Barakat-Walter I & Droz B (1994). Innervation of putative rapidly adapting mechanoreceptors by calbindin- and calretinin-immunoreactive primary sensory neurons in the rat. Eur J Neurosci 6, 264-271.
20. El-Tarhouni A & Banks RW (1995). The distribution of calretinin in muscle receptors of the cat. J Physiol 487.P, 77P.
21. Engberg I, Tarnawa I, Durand J & Ouardouz M (1993). An analysis of synaptic transmission to motoneurons in the cat spinal-cord using a new selective receptor blocker. Acta Physiol Scand 148 97-100.
22. Gale JE, Marcotti W, Kennedy HJ, Kros CJ & Richardson GP (2001). FM1-43 dye behaves as a permeant blocker of the hair-cell mechanotransducer channel. J Neurosci 21, 7013-7025.
23. Griesinger CB, Richards CD & Ashmore JF (2002). FM1-43 reveals membrane recycling in adult inner hair cells of the mammalian cochlea. J Neurosci 22, 3939-3952.
24. Hamill OP & Martinac B (2001). Molecular basis of mechanotransduction in living cells. Physiol Rev 81, 685-740.
25. Hietanen-Peltola M, Pelto-Huikko M, Rechardt L, Emson P & Hökfelt T (1992). Calbindin-D-28k-immunoreactivity in rat muscle spindle; a light and electron microscopic study. Brain Res 579 327-332.
26. Hunt CC, Wilkinson RS & Fukami Y (1978). Ionic basis of the receptor potential in primary endings of mammalian muscle spindles. J General Physiol 71, 683-698.
27. Iggo A (1974). Cutaneous receptors. In The Peripheral Nervous System, ed. Hubbard JI, pp. 347-404. Plenum Press, New York.
28. Iino S, Kobayashi S & Hidaka H (1998). Neurocalcin-immunopositive nerve terminals in the muscle spindle, Golgi tendon organ and motor endplate. Brain Res 808, 294-299.
29. Iino S, Taguchi K & Maekawa Si & Nojyo Y (2004). Motor, sensory and autonomic nerve terminals containing NAP-22 immunoreactivity in the rat muscle. Brain Res 1002, 142-150.
30. Ito I, Kohda A, Tanabe S, Hirose E, Hayashi M et al. (1992). 3,5-Dihydroxyphenylglycine - a potent agonist of metabotropic glutamate receptors. Neuroreport 3, 1013-1016.
31. Kilner JM & Ashmore JF (1997). Staining pattern of isolated inner hair cells of the guinea-pig cochlea using the fluorescent probe FM1-43. J Physiol 504.P, 30-31P.
32. Kruse MN & Poppele RE (1991). Components of the dynamic response of mammalian muscle spindles that originate in the sensory terminals. Exp Brain Res 86, 359-366.
33. Li J-Y, Edelmann L, Jahn R & Dahlström A (1996). Axonal transport and distribution of synaptobrevin I and II in the rat peripheral nervous system. J Neurosci 16, 137-147.
34. Liley AW (1956). An investigation of spontaneous activity at the neuromuscular junction of the rat. J Physiol 132, 650-666.
35. Matthews PBC (1972). Mammalian Muscle Receptors and Their Central Actions. Edward Arnold, London.
36. Mizote M & Takano K (1985). The response of cat muscle spindle primary endings to FM muscle vibration during fusimotor stimulation or following local injection of tetanus toxin. In The Muscle Spindle, ed. Boyd IA & Gladden MH, pp. 365-369. Macmillan Press, London.
37. Moravec M & Moravec J (1982). Presence of mechanoreceptors in the atrioventricular junction of the rat-heart - microanatomical and ultrastructural evidences. J Utrastruct Res 81, 47-65.
38. Munger BL & Ide C (1988). The structure and function of cutaneous sensory receptors. Arch Histol Cytol 51, 1-34.
39. Nishikawa S & Sasaki F (1996). Internalization of styryl dye FM1-43 in the hair cells of lateral line organs in Xenopus larvae. J Histochem Cytochem 44, 733-741.
40. Pellegrini-Giampietro DE, Torregrossa SA & Moroni F (1996). Pharmacological characterization of metabotropic glutamate receptors coupled to phospholipase D in the rat hippocampus. Br J Pharmacol 118, 1035-1043.
41. Pellizari R, Rossetto O, Schiavo G & Montecucco C (1999). Tetanus and botulinum neurotoxins: mechanism of action and therapeutic uses. Phil Trans R Soc Lond B 354, 259-268.
42. Poppele RE, Kennedy WR & Quick DC (1979). A determination of static mechanical properties of intrafusal muscle in isolated cat spindles. Neuroscience 4, 401-411.
43. Queiroz LS & Duchen LW (1982). Effects of Latrodectus spider venoms on sensory and motor-nerve terminals of muscle-spindles. Proc R Soc Lond B 216, 103-110.
44. Sidi S, Friedrich RW & Nicolson T (2003). NompC TRP channel required for vertebrate sensory hair cell mechanotransduction. Science 301, 96-99.
45. Somogyi P, Halasy K, Somogyi J, Storm-Mathisen J & Ottersen OP (1986). Quantification of immunogold labelling reveals enrichment of glutamate in mossy and parallel fibre terminals in cat cerebellum. Neuroscience 19, 1045-1050.
46. Storm-Mathisen J, Leknes AK, Bore AT, Vaaland JL, Edminson P et al. (1983). First visualization of glutamate and GABA in neurons by immunocytochemistry. Nature 301, 517-520.
47. Ushkaryov YA, Volynski KE & Ashton AC (2004). The multiple actions of black widow spider toxins and their selective use in neurosecretion studies. Toxicon 43, 527-542.
48. Walmsley B & Bolton PS (1994). An in-vivo pharmacological study of single group-Ia fiber contacts with motoneurons in the cat spinal-cord. J Physiol 481, 731-741.
49. + channels. J Biol Chem 277, 2369-2372.
50. Werle MJ, Roder J & Jeromin A (2000). Expression of frequenin at the frog (Rana) neuromuscular junction, muscle spindle and nerve. Neurosci Lett 284, 33-36.
51. Widdicombe JG (1974). Enteroceptors. In The Peripheral Nervous System, ed. Hubbard JI, pp. 455-485. Plenum Press, New York.
52. Wu S-X, Koshimizu Y, Feng Y-P, Okamoto K, Fujiyama F, et al. (2004). Vesicular glutamate transporter immunoreactivity in the central and peripheral endings of muscle-spindle afferents. Brain Res 1011, 247-251.
53. Zelená J (1994). Nerves and Mechanoreceptors. Chapman & Hall, London.