Long-term effects of botulinum toxin complex type a injection on mechano-and metabo-sensitive afferent fibers originating from gastrocnemius muscle

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Caron, Guillaume ^a   Marqueste, Tanguy ^a   Decherchi, Patrick ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BOTULINUM TOXIN A; LACTIC ACID; NEUROTOXIN; POTASSIUM CHLORIDE;

ACHILLES TENDON; ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSOL; ELECTRICALLY INDUCED FATIGUE; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; GASTROCNEMIUS MUSCLE; LOCOMOTION; MALE; MECHANOSENSITIVE AFFERENT FIBER; METABOSENSITIVE AFFERENT FIBER; MOTOR ACTIVITY; MUSCLE ATROPHY; MUSCLE DENERVATION; MUSCLE EXCITATION; MUSCLE FATIGUE; MUSCLE MASS; MUSCLE SPINDLE AFFERENT NERVE; MUSCLE TWITCH; MUSCULOSKELETAL SYSTEM PARAMETERS; NONHUMAN; PARALYSIS; RAT; TETANUS THRESHOLD; VIBRATION; ANIMAL; CONVALESCENCE; DRUG EFFECTS; HINDLIMB; INNERVATION; INTRAMUSCULAR DRUG ADMINISTRATION; MUSCLE CONTRACTION; PHYSIOLOGY; SENSORY NERVE; SENSORY NERVE CELL; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT; TENDON; TIME FACTOR;

AFFERENT PATHWAYS; ANIMALS; BOTULINUM TOXINS, TYPE A; ELECTRIC STIMULATION; ELECTROPHYSIOLOGICAL PHENOMENA; HINDLIMB; INJECTIONS, INTRAMUSCULAR; LACTIC ACID; MALE; MOTOR ACTIVITY; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE, SKELETAL; NEURONS, AFFERENT; NEUROTOXINS; POTASSIUM CHLORIDE; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; TENDONS; TIME FACTORS;

EID: 84948970492     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0140439     Document Type: Article

References (118)

1. Dressler D, Rothwell JC (2000) Electromyographic quantification of the paralysing effect of botulinum toxin in the sternocleidomastoid muscle. Eur Neurol 43:13-16. PMID: 10798896
2. Rizo J, Sudhof TC(2002) Snares and Munc18in synaptic vesicle fusion. Nat Rev Neurosci 3: 641-653. PMID: 12154365
3. Hallett M, Glocker FX, Deuschl G (1994) Mechanism of action of botulinum toxin. Ann Neurol 36: 449-450. PMID: 8080256
4. Curra A, Trompetto C, Abbruzzese G, Berardelli A (2004) Central effects of botulinum toxin type A: evidence and supposition. Mov Disord 19Suppl8: S60-64. PMID: 15027056
5. Abbruzzese G, Berardelli A (2006) Neurophysiological effects of botulinum toxin type A. Neurotox Res 9:109-114. PMID: 16785106
6. Caleo M, Schiavo G (2009) Central effects of tetanus and botulinum neurotoxins. Toxicon 54: 593-599. doi: 10.1016/j.toxicon.2008.12.026 PMID: 19264088
7. Cui M, Khanijou S, Rubino J, Aoki KR (2004) Subcutaneous administration of botulinum toxin A reduces formalin-induced pain. Pain 107:125-133. PMID: 14715398
8. Welch MJ, Purkiss JR, Foster KA (2000) Sensitivity of embryonic rat dorsal root ganglia neurons to Clostridium botulinum neurotoxins. Toxicon 38: 245-258. PMID: 10665805
9. Lucioni A, Bales GT, Lotan TL, McGehee DS, Cook SP, et al. (2008) Botulinum toxin type A inhibits sensory neuropeptide release in rat bladder models of acute injury and chronic inflammation. BJU Int 101: 366-370. doi: 10.1111/j.1464-410X.2007.07312.x PMID: 18184328
10. Meng J, Wang J, Lawrence G, Dolly JO (2007) Synaptobrevin I mediates exocytosis of CGRP from sensory neurons and inhibition by botulinum toxins reflects their anti-nociceptive potential. J Cell Sci 120: 2864-2874. PMID: 17666428
11. Verderio C, Grumelli C, Raiteri L, Coco S, Paluzzi S, et al. (2007) Traffic of botulinum toxins A and Ein excitatory and inhibitory neurons. Traffic 8:142-153. PMID: 17241445
12. Wiegand H, Erdmann G, Wellhoner HH (1976) 125I-labelled botulinum A neurotoxin: pharmacokinetics in cats after intramuscular injection. Naunyn Schmiedebergs Arch Pharmacol 292:161-165. PMID: 59905
13. Kim DY, Oh BM, Paik NJ (2006) Central effect of botulinum toxin type A in humans. Int J Neurosci 116: 667-680. PMID: 16753894
14. Antonucci F, Rossi C, Gianfranceschi L, Rossetto O, Caleo M (2008) Long-distance retrograde effects of botulinum neurotoxin A. J Neurosci 28: 3689-3696. doi: 10.1523/JNEUROSCI.0375-08.2008 PMID: 18385327
15. Filippi GM, Errico P, Santarelli R, Bagolini B, Manni E (1993) Botulinum A toxin effects on rat jaw muscle spindles. Acta Otolaryngol 113:400-404. PMID: 8390772
16. Rosales RL, Arimura K, Takenaga S, Osame M (1996) Extrafusal and intrafusal muscle effects in experimental botulinum toxin-A injection. Muscle Nerve 19: 488-496. PMID: 8622728
17. Priori A, Berardelli A, Mercuri B, Manfredi M (1995) Physiological effects produced by botulinum toxin treatment of upper limb dystonia. Changes in reciprocal inhibition between forearm muscles. Brain 118 (Pt3): 801-807. PMID: 7600096
18. Rosales RL, Dressler D (2010) On muscle spindles, dystonia and botulinum toxin. Eur J Neurol 17 Suppl 1: 71-80. doi: 10.1111/j.1468-1331.2010.03056.x PMID: 20590812
19. Caron G, Rouzi T, Grelot L, Magalon G, Marqueste T, et al. (2014) Mechano-and metabosensitive alterations after injection of botulinum toxin into gastrocnemius muscle. J Neurosci Res 92: 904-914. doi: 10.1002/jnr.23370 PMID: 24615939
20. Pierrot-Deseilligny E, Burke D (2005) The circuit of the Human Spinal Cord: Its Role in Motor Control and Movement Disorders. New York: Cambrige University Press.
21. Brown MC, Engberg I, Matthews PB (1967) The relative sensitivity to vibration of muscle receptors of the cat. J Physiol 192: 773-800. PMID: 4293790
22. Brown AG, Iggo A (1967) A quantitative study of cutaneous receptors and afferent fibres in the cat and rabbit. J Physiol 193: 707-733. PMID: 16992307
23. Brown AG, Iggo A, Miller S (1967) Myelinated afferent nerve fibers from the skin of the rabbit ear. Exp Neurol 18: 338-349. PMID: 6028148
24. Kaufman MP, Rybicki KJ (1987) Discharge properties of group III and IV muscle afferents: their responses to mechanical and metabolic stimuli. Circ Res 61:I60-65. PMID: 3652404
25. Rotto DM, Kaufman MP (1988) Effect of metabolic products of muscular contraction on discharge of group III and IVafferents. J Appl Physiol 64: 2306-2313. PMID: 3136123
26. Ge W, Khalsa PS (2003) Encoding of compressive stress during indentation by group III and IV muscle mechano-nociceptors in rat gracilis muscle. J Neurophysiol 89: 785-792. PMID: 12574456
27. Decherchi P, Darques JL, Jammes Y (1998) Modifications of afferent activities from Tibialis anterior muscle in rat by tendon vibrations, increase of interstitial potassium or lactate concentration and electrically-induced fatigue. J Peripher Nerv Syst 3: 267-276. PMID: 10970127
28. Kaufman MP, Iwamoto GA, Longhurst JC, Mitchell JH (1982) Effects of capsaicin and bradykinin on afferent fibers with ending in skeletal muscle. Circ Res 50:133-139. PMID: 7053873
29. Victor RG, Bertocci LA, Pryor SL, Nunnally RL(1988) Sympathetic nerve discharge is coupled to muscle cell pH during exercise in humans. J Clin Invest 82:1301-1305. PMID: 3170747
30. Kenagy J, Van Cleave J, Pazdernik L, Orr JA(1997) Stimulation of group III and IV afferent nerves from the hindlimb by thromboxane A2. Brain Res 744:175-178. PMID: 9030430
31. Rybicki KJ, Waldrop TG, Kaufman MP (1985) Increasing gracilis muscle interstitial potassium concentrations stimulate group III and IV afferents. J Appl Physiol 58: 936-941. PMID: 2984167
32. Decherchi P, Vuillon-Cacciutolo G, Darques JL, Jammes Y (2001) Changes in afferent activities from tibialis anterior muscle after nerve repair by self-anastomosis. Muscle Nerve 24: 59-68. PMID: 11150967
33. Holds JB, Fogg SG, Anderson RL (1990) Botulinum A toxin injection. Failures in clinical practice and a biomechanical system for the study of toxin-induced paralysis. Ophthal Plast Reconstr Surg 6: 252-259. PMID: 2271481
34. Hott JS, Dalakas MC, Sung C, Hallett M, Youle RJ (1998) Skeletal muscle-specific immunotoxin for the treatment of focal muscle spasm. Neurology 50:485-491. PMID: 9484377
35. Billante CR, Zealear DL, Billante M, Reyes JH, Sant'Anna G, et al. (2002) Comparison of neuromuscular blockade and recovery with botulinum toxins A and F. Muscle Nerve 26: 395-403. PMID: 12210370
36. Varejao AS, Cabrita AM, Patricio JA, Bulas-Cruz J, Gabriel RC, et al. (2001) Functional assessment of peripheral nerve recovery in the rat: gait kinematics. Microsurgery 21: 383-388. PMID: 11757066
37. Bain JR, Mackinnon SE, Hunter DA (1989) Functional evaluation of complete sciatic, peroneal, and posterior tibial nerve lesions in the rat. Plast Reconstr Surg 83:129-138. PMID: 2909054
38. de Medinaceli L, Freed WJ, Wyatt RJ (1982) An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks. Exp Neurol 77: 634-643. PMID: 7117467
39. Hruska RE, Kennedy S, Silbergeld EK (1979) Quantitative aspects of normal locomotion in rats. Life Sci 25:171-179. PMID: 491843
40. Kostyukov AI, Hellstrom F, Korchak OE, Radovanovic S, Ljubisavljevic M, et al. (2000) Fatigue effects in the cat gastrocnemius during frequency-modulated efferent stimulation. Neuroscience 97: 789-799. PMID: 10842025
41. Lopez-Guajardo A, Sutherland H, Jarvis JC, Salmons S (2001) Induction of a fatigue-resistant pheno-typein rabbit fast muscle by small daily amounts of stimulation. J Appl Physiol (1985) 90:1909-1918.
42. Kaufman MP, Waldrop TG, Rybicki KJ, Ordway GA, Mitchell JH (1984) Effects of static and rhythmic twitch contractions on the discharge of group III and IV muscle afferents. Cardiovasc Res 18: 663-668. PMID: 6498873
43. Burke D, Schiller HH (1976) Discharge pattern of single motor units in the tonic vibration reflex of human triceps surae. J Neurol Neurosurg Psychiatry 39: 729-741. PMID: 956859
44. Roll JP, Vedel JP, Ribot E (1989) Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographicstudy. Exp Brain Res 76: 213-222. PMID: 2753103
45. Sloop RR, Cole BA, Escutin RO (1997) Human response to botulinum toxin injection: type B compared with type A. Neurology 49:189-194. PMID: 9222189
46. Ma J, Elsaidi GA, Smith TL, Walker FO, Tan KH, et al. (2004) Time course of recovery of juvenile skeletal muscle after botulinum toxin A injection: an animal model study. Am J Phys Med Rehabil 83: 774-780; quiz 781-773. PMID: 15385786
47. Keller JE(2006) Recoveryfrom botulinum neurotoxin poisoningin vivo. Neuroscience 139:629-637. PMID: 16490322
48. Duchen LW (1971) Changes in the electron microscopic structure of slow and fast skeletal muscle fibres ofthe mouse afterthe local injection of botulinum toxin. J Neurol Sci 14:61-74. PMID: 5119452
49. Duchen LW (1971) An electron microscopic study of the changes induced by botulinum toxin in the motor end-plates of slow and fast skeletal muscle fibres of the mouse. J Neurol Sci 14: 47-60. PMID: 5119451
50. Dodd SL, Selsby J, Payne A, Judge A, Dott C (2005) Botulinum neurotoxin type A causes shifts in myosin heavy chain composition in muscle. Toxicon 46:196-203. PMID: 15975617
51. Legerlotz K, Matthews KG, McMahon CD, Smith HK (2009) Botulinum toxin-induced paralysis leads to slower myosin heavy chain isoform composition and reduced titin content in juvenile rat gastrocnemius muscle. Muscle Nerve 39: 472-479. doi: 10.1002/mus.21247 PMID: 19260067
52. Delp MD, Duan C (1996) Composition and size of type I, IIA, IID/X, and IIB fibers and citrate synthase activity of rat muscle. J Appl Physiol (1985) 80: 261-270.
53. Duchateau J, Hainaut K (1990) Effects of immobilization on contractile properties, recruitment and firing rates of human motor units. J Physiol 422: 55-65. PMID: 2352193
54. Yu BP, Masoro EJ, Murata I, Bertrand HA, Lynd FT (1982) Lifespan study of SPF Fischer 344 male rats fed ad libitum or restricted diets: longevity, growth, lean body mass and disease. J Gerontol 37: 130-141. PMID: 7056998
55. Cartee GD (1994) Aging skeletal muscle: response to exercise. Exerc Sport Sci Rev 22: 91-120. PMID: 7925554
56. Chiu CS, Weber H, Adamski S, Rauch A, Gentile MA, et al. (2011) Non-invasive muscle contraction assay to study rodent models of sarcopenia. BMC Musculoskelet Disord 12: 246. doi: 10.1186/1471-2474-12-246 PMID: 22035016
57. Kaufman MP, Forster H (1996) Reflexes controlling circulatory, ventilatory and airway responses to exercise.; Rowell LB, Shepherd JT, editors. New York: Oxford University Press.
58. Marqueste T, Decherchi P, Dousset E, Berthelin F, Jammes Y (2002) Effect of muscle electrostimulation on afferent activities from tibialis anterior muscle after nerve repair by self-anastomosis. Neuroscience 113: 257-271. PMID: 12127084
59. Dousset E, Marqueste T, Decherchi P, Jammes Y, Grelot L (2004) Effects of neonatal capsaicin deaf-ferentation on neuromuscular adjustments, performance, and afferent activities from adult tibialis anterior muscle during exercise. J Neurosci Res 76: 734-741. PMID: 15139032
60. Thimm F, Baum K(1987) Response of chemosensitive nerve fibers of group III and IV to metabolic changes in rat muscles. Pflugers Arch 410:143-152. PMID: 3684503
61. Darques JL, Jammes Y(1997) Fatigue-induced changes in group IV muscle afferent activity: differences between high-and low-frequency electrically induced fatigues. Brain Res 750:147-154. PMID: 9098539
62. Mense S, Prabhakar NR(1986) Spinal termination of nociceptive afferent fibres from deep tissues in the cat. Neurosci Lett 66:169-174. PMID: 3725183
63. Hnik P, Holas M, Krekule I, Kuriz N, Mejsnar J, et al. (1976) Work-induced potassium changes in skeletal muscle and effluent venous blood assessed by liquid ion-exchanger microelectrodes. Pflugers Arch 362: 85-94. PMID: 943782
64. Gao Z, Henig O, Kehoe V, Sinoway LI, Li J (2006) Vanilloid type 1 receptor and the acid-sensing ion channel mediate acid phosphate activation of muscle afferent nerves in rats. J Appl Physiol (1985) 100: 421-426.
65. Apostolidis A, Popat R, Yiangou Y, Cockayne D, Ford AP, et al. (2005) Decreased sensory receptors P2X3 and TRPV1 in suburothelial nerve fibers following intradetrusor injections of botulinum toxin for human detrusor overactivity. J Urol 174: 977-982; discussion 982-973. PMID: 16094018
66. Shimizu T, Shibata M, Toriumi H, Iwashita T, Funakubo M, et al. (2012) Reduction of TRPV1 expression in the trigeminal system by botulinum neurotoxin type-A. Neurobiol Dis 48: 367-378. doi: 10.1016/j.nbd.2012.07.010 PMID: 22820141
67. Darques JL, Decherchi P, Jammes Y (1998) Mechanisms of fatigue-induced activation of group IV muscle afferents: the roles played by lactic acid and inflammatory mediators. Neurosci Lett 257:109-112. PMID: 9865939
68. Marqueste T, Decherchi P, Messan F, Kipson N, Grelot L, et al. (2004) Eccentric exercise alters muscle sensory motor control through the release of inflammatory mediators. Brain Res 1023: 222-230. PMID: 15374748
69. Carmichael NM, Dostrovsky JO, Charlton MP (2010) Peptide-mediated transdermal delivery of botulinum neurotoxin type A reduces neurogenic inflammation in the skin. Pain 149: 316-324. doi: 10.1016/j.pain.2010.02.024 PMID: 20223589
70. Smith SA, Mitchell JH, Garry MG (2006) The mammalian exercise pressor reflex in health and disease. Exp Physiol 91: 89-102. PMID: 16282366
71. Smith SA, Mitchell JH, Naseem RH, Garry MG (2005) Mechanoreflex mediates the exaggerated exercise pressor reflex in heart failure. Circulation 112: 2293-2300. PMID: 16216976
72. Lynch GS, Ryall JG (2008) Role of beta-adrenoceptor signaling in skeletal muscle: implications for muscle wasting and disease. Physiol Rev 88: 729-767. doi: 10.1152/physrev.00028.2007 PMID: 18391178
73. Caswell AH, Baker SP, Boyd H, Potter LT, Garcia M (1978) beta-adrenergic receptor and adenylate cyclase in transverse tubules of skeletal muscle. J Biol Chem 253: 3049-3054. PMID: 205539
74. Barker D, Saito M (1981) Autonomic innervation of receptors and muscle fibres in cat skeletal muscle. Proc R Soc Lond B Biol Sci 212: 317-332. PMID: 6115396
75. Rattigan S, Appleby GJ, Edwards SJ, McKinstry WJ, Colquhoun EQ, et al. (1986) Alpha-adrenergic receptors in rat skeletal muscle. Biochem Biophys Res Commun 136:1071-1077. PMID: 3013164
76. Akaike N, Hirata A, Kiyohara T, Oyama Y (1983) Neural regulation on the active sodium-potassium transport in hypokalaemic rat skeletal muscles. J Physiol 341: 245-255. PMID: 6137559
77. Kim YS, Sainz RD, Molenaar P, Summers RJ (1991) Characterization of beta 1-and beta 2-adreno-ceptors in rat skeletal muscles. Biochem Pharmacol 42:1783-1789. PMID: 1681810
78. Williams RS, Caron MG, Daniel K (1984) Skeletal muscle beta-adrenergic receptors: variations due to fibertype and training. Am J Physiol 246: E160-167. PMID: 6320672
79. Ryall JG, Gregorevic P, Plant DR, Sillence MN, Lynch GS(2002) Beta 2-agonist fenoterol has greater effects on contractile function of rat skeletal muscles than clenbuterol. Am J Physiol Regul Integr Comp Physiol 283: R1386-1394. PMID: 12388476
80. Ryall JG, Plant DR, Gregorevic P, Sillence MN, Lynch GS (2004) Beta 2-agonist administration reverses muscle wasting and improves muscle function in aged rats. J Physiol 555:175-188. PMID: 14617677
81. Martin WH3rd, Murphree SS, Saffitz JE (1989) Beta-adrenergic receptor distribution among muscle fiber types and resistance arterioles of white, red, and intermediate skeletal muscle. Circ Res 64: 1096-1105. PMID: 2541942
82. Buckwalter JB, Clifford PS (2001) The paradox of sympathetic vasoconstriction in exercising skeletal muscle. Exerc Sport Sci Rev 29:159-163. PMID: 11688788
83. Apseloff G, Girten B, Walker M, Shepard DR, Krecic ME, et al. (1993) Aminohydroxybutane bisphos-phonate and clenbuterol prevent bone changes and retard muscle atrophy respectively in tail-suspended rats. J Pharmacol Exp Ther 264:1071-1078. PMID: 8450451
84. Hinkle RT, Hodge KM, Cody DB, Sheldon RJ, Kobilka BK, et al. (2002) Skeletal muscle hypertrophy and anti-atrophy effects of clenbuterol are mediated by the beta2-adrenergic receptor. Muscle Nerve 25: 729-734. PMID: 11994968
85. Mersmann HJ (1998) Overview of the effects of beta-adrenergic receptor agonists on animal growth including mechanisms of action. J Anim Sci 76:160-172. PMID: 9464897
86. Sato S, Shirato K, Tachiyashiki K, Imaizumi K (2011) Muscle plasticity and beta(2)-adrenergic receptors: adaptive responses of beta(2)-adrenergic receptor expression to muscle hypertrophy and atrophy. J Biomed Biotechnol 2011: 729598. doi: 10.1155/2011/729598 PMID: 22190857
87. Berecek KH, Brody MJ (1982) Evidence for a neurotransmitter role for epinephrine derived from the adrenal medulla. Am J Physiol 242: H593-601. PMID: 6278965
88. Burniston JG, Tan LB, Goldspink DF (2005) beta2-Adrenergic receptor stimulation in vivo induces apoptosis in the rat heart and soleus muscle. J Appl Physiol (1985) 98:1379-1386.
89. Burniston JG, Clark WA, Tan LB, Goldspink DF (2006) Dose-dependent separation of the hypertrophic and myotoxic effects of the beta(2)-adrenergic receptor agonist clenbuterol in rat striated muscles. Muscle Nerve 33: 655-663. PMID: 16411205
90. McCloskey DI, Mitchell JH (1972) Reflex cardiovascular and respiratory responses originating in exercising muscle. J Physiol 224:173-186. PMID: 5039977
91. Kaur J, Spranger MD, Hammond RL, Krishnan AC, Alvarez A, et al. (2014) Muscle metaboreflex activation during dynamic exercise evokes epinephrine release resulting in beta2-mediated vasodilation. Am J Physiol Heart Circ Physiol: ajpheart 00648 02014.
92. Fromm C, Haase J, Wolf E (1977) Depression of the recurrent inhibition of extensor motoneurons by the action of group II afferents. Brain Res 120: 459-468. PMID: 832135
93. Hagbarth KE, Eklund G (1966) Tonic vibration reflexes (TVR) in spasticity. Brain Res 2: 201-203. PMID: 5968925
94. De Gail P, Lance JW, Neilson PD (1966) Differential effects on tonic and phasic reflex mechanisms produced by vibration of muscles in man. J Neurol Neurosurg Psychiatry 29:1-11. PMID: 5910574
95. Albuquerque EX, Thesleff S (1968) A comparative study of membrane properties of innervated and chronically denervated fast and slow skeletal muscles of the rat. Acta Physiol Scand 73: 471-480. PMID: 5708174
96. Albuquerque EX, Schuh FT, Kauffman FC(1971) Early membrane depolarization of the fast mammalian muscle after denervation. Pflugers Arch 328: 36-50. PMID: 4331161
97. Lewis GE (1981) Biomedical aspects of botulism. London: Academic Press Inc.
98. Sellin LC, Thesleff S (1981) Pre-and post-synaptic actions of botulinum toxin at the rat neuromuscular junction. J Physiol 317: 487-495. PMID: 6273549
99. Tonge DA (1974) Chronic effects of botulinum toxin on neuromuscular transmission and sensitivity to acetylcholine in slow and fast skeletal muscle of the mouse. J Physiol 241:127-139. PMID: 4371301
100. Paterson K, Lolignier S, Wood JN, McMahon SB, Bennett DL (2014) Botulinum toxin-A treatment reduces human mechanical pain sensitivity and mechanotransduction. Ann Neurol 75: 591-596. doi: 10.1002/ana.24122 PMID: 24550077
101. Drew LJ, Rugiero F, Cesare P, Gale JE, Abrahamsen B, et al. (2007) High-threshold mechanosensi-tive ion channels blocked by a novel conopeptide mediate pressure-evoked pain. PLoS One 2: e515. PMID: 17565368
102. Vilceanu D, Stucky CL (2010) TRPA1 mediates mechanical currents in the plasma membrane of mouse sensory neurons. PLoS One 5: e12177. doi: 10.1371/journal.pone.0012177 PMID: 20808441
103. Kerstein PC, delCamino D, Moran MM, Stucky CL (2009) Pharmacological blockade of TRPA1 inhibits mechanical firing in nociceptors. Mol Pain 5:19. doi: 10.1186/1744-8069-5-19 PMID: 19383149
104. Rugiero F, Wood JN (2009) The mechanosensitive cell line ND-Cdoes not express functional ther-moTRP channels. Neuropharmacology 56:1138-1146. doi: 10.1016/j.neuropharm.2009.03.012 PMID: 19348834
105. Di Castro A, Drew LJ, Wood JN, Cesare P(2006) Modulation of sensory neuron mechanotransduction by PKC-and nerve growth factor-dependent pathways. Proc Natl Acad Sci USA 103: 4699-4704. PMID: 16537426
106. Bewick GS, Banks RW(2015) Mechanotransduction in the muscle spindle. Pflugers Arch 467:175-190. doi: 10.1007/s00424-014-1536-9 PMID: 24888691
107. Aguado F, Majo G, Ruiz-Montasell B, Llorens J, Marsal J, et al. (1999)Syntaxin 1Aand 1B display distinct distribution patterns in the rat peripheral nervous system. Neuroscience 88: 437-446. PMID: 10197765
108. Koriazova LK, Montal M (2003) Translocation of botulinum neurotoxin light chain protease through the heavy chain channel. Nat Struct Biol 10:13-18. PMID: 12459720
109. Fischer A, Montal M (2007) Crucial role of the disulfide bridge between botulinum neurotoxin light and heavy chains in protease translocation across membranes. J Biol Chem 282: 29604-29611. PMID: 17666397
110. Simpson L (2013) The life history of a botulinum toxin molecule. Toxicon 68: 40-59. doi: 10.1016/j. toxicon.2013.02.014 PMID: 23518040
111. Ravichandran E, Gong Y, Al Saleem FH, Ancharski DM, Joshi SG, et al. (2006) An initial assessment of the systemic pharmacokinetics of botulinum toxin. J Pharmacol Exp Ther 318:1343-1351. PMID: 16782822
112. Shoemaker CB, Oyler GA (2013) Persistence of Botulinum neurotoxin inactivation of nerve function. Curr Top Microbiol Immunol 364:179-196. doi: 10.1007/978-3-642-33570-9 9 PMID: 23239354
113. Takimoto E, Champion HC, Li M, Belardi D, Ren S, et al. (2005) Chronic inhibition of cyclic GMP phosphodiesterase 5A prevents and reverses cardiac hypertrophy. Nat Med 11: 214-222. PMID: 15665834
114. Akaike N, Shin MC, Wakita M, Torii Y, Harakawa T, et al. (2013) Transsynaptic inhibition of spinal transmission byA2 botulinum toxin. J Physiol 591:1031-1043. doi: 10.1113/jphysiol.2012.242131 PMID: 23109108
115. Koizumi H, Goto S, Okita S, Morigaki R, Akaike N, et al. (2014) Spinal Central Effects of Peripherally Applied Botulinum Neurotoxin A in Comparison between Its Subtypes A1 and A2. Front Neurol 5: 98. doi: 10.3389/fneur.2014.00098 PMID: 25002857
116. Purkiss JR, Welch MJ, Doward S, Foster KA (1997) Capsaicin stimulates release of substance Pfrom dorsal root ganglion neurons via two distinct mechanisms. Biochem Soc Trans 25: 542S. PMID: 9388756
117. Purkiss J, Welch M, Doward S, Foster K (2000) Capsaicin-stimulated release of substance Pfrom cultured dorsal root ganglion neurons: involvement of two distinct mechanisms. Biochem Pharmacol 59: 1403-1406. PMID: 10751549
118. Aoki KR(2005) Review of a proposed mechanism for the antinociceptive action of botulinum toxin type A. Neurotoxicology 26:785-793. PMID: 16002144