Botulinum toxin B in the sensory afferent: Transmitter release, spinal activation, and pain behavior

Pain

Volumn 155, Issue 4, 2014, Pages 674-684

  Marino, Marc J ^a   Terashima, Tetsuji ^b   Steinauer, Joanne J ^a   Eddinger, Kelly A ^a   Yaksh, Tony L ^a   Xu, Qinghao ^a  

^a University of California   (United States)

^b DOKKYO MEDICAL UNIVERSITY   (Japan)

Author keywords

Botulinum toxin; Dorsal root ganglion; Neurotransmitter release; Sensory afferent; Spinal cord; Substance P; VAMP

Indexed keywords

BOTULINUM TOXIN B; CAPSAICIN; NEUROKININ 1 RECEPTOR; PROTEIN C FOS; SYNAPTOBREVIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DRUG MECHANISM; MALE; MOTOR PERFORMANCE; MOUSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PAIN; PAIN THRESHOLD; PRIORITY JOURNAL; SENSORY NERVE; SPINAL CORD DORSAL HORN; SPINAL GANGLION;

BOTULINUM TOXIN; DORSAL ROOT GANGLION; NEUROTRANSMITTER RELEASE; SENSORY AFFERENT; SPINAL CORD; SUBSTANCE P; VAMP;

AFFERENT PATHWAYS; ANIMALS; ANTI-DYSKINESIA AGENTS; BOTULINUM TOXINS; CAPSAICIN; FUNCTIONAL LATERALITY; GENE EXPRESSION REGULATION; HINDLIMB SUSPENSION; MALE; MICE; MICE, INBRED C57BL; MUSCLE STRENGTH; NOCICEPTORS; PAIN; PAIN THRESHOLD; POSTERIOR HORN CELLS; RECEPTORS, NEUROKININ-1; SPINAL CORD; SUBSTANCE P; TIME FACTORS;

EID: 84896403633     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2013.12.009     Document Type: Article

References (109)

1. N. Akaike, M.C. Shin, M. Wakita, Y. Torii, T. Harakawa, A. Ginnaga, K. Kato, R. Kaji, and S. Kozaki Transsynaptic inhibition of spinal transmission by A2 botulinum toxin J Physiol 591 2013 1031 1043
2. S. Anderson, H. Krug, C. Dorman, P. McGarraugh, S. Frizelle, and M. Mahowald Analgesic effects of intra-articular botulinum toxin Type B in a murine model of chronic degenerative knee arthritis pain J Pain Res 3 2010 161 168
3. T. Andoh, T. Nagasawa, and Y. Kuraishi Expression of tachykinin NK1 receptor mRNA in dorsal root ganglia of the mouse Brain Res Mol Brain Res 35 1996 329 332
4. P.V. Andrews, R.D. Helme, and K.L. Thomas NK-1 receptor mediation of neurogenic plasma extravasation in rat skin Br J Pharmacol 97 1989 1232 1238
5. F. Antonucci, C. Rossi, L. Gianfranceschi, O. Rossetto, and M. Caleo Long-distance retrograde effects of botulinum neurotoxin A J Neurosci 28 2008 3689 3696
6. K.R. Aoki Botulinum neurotoxin serotypes A and B preparations have different safety margins in preclinical models of muscle weakening efficacy and systemic safety Toxicon 40 2002 923 928
7. L. Bach-Rojecky, M. Dominis, and Z. Lackovic Lack of anti-inflammatory effect of botulinum toxin type A in experimental models of inflammation Fundam Clin Pharmacol 22 2008 503 509
8. L. Bach-Rojecky, and Z. Lackovic Antinociceptive effect of botulinum toxin type a in rat model of carrageenan and capsaicin induced pain Croat Med J 46 2005 201 208
9. L. Bach-Rojecky, and Z. Lackovic Central origin of the antinociceptive action of botulinum toxin type A Pharmacol Biochem Behav 94 2009 234 238
10. L. Bach-Rojecky, M. Salkovic-Petrisic, and Z. Lackovic Botulinum toxin type A reduces pain supersensitivity in experimental diabetic neuropathy: bilateral effect after unilateral injection Eur J Pharmacol 633 2010 10 14
11. T. Binz, S. Sikorra, and S. Mahrhold Clostridial neurotoxins: mechanism of SNARE cleavage and outlook on potential substrate specificity reengineering Toxins (Basel) 2 2010 665 682
12. W. Blersch, W.J. Schulte-Mattler, S. Przywara, A. May, H. Bigalke, and K. Wohlfarth Botulinum toxin A and the cutaneous nociception in humans: a prospective, double-blind, placebo-controlled, randomized study J Neurol Sci 205 2002 59 63
13. F.C. Blum, C. Chen, A.R. Kroken, and J.T. Barbieri Tetanus toxin and botulinum toxin a utilize unique mechanisms to enter neurons of the central nervous system Infect Immun 80 2012 1662 1669
14. J.L. Brown, H. Liu, J.E. Maggio, S.R. Vigna, P.W. Mantyh, and A.I. Basbaum Morphological characterization of substance P receptor-immunoreactive neurons in the rat spinal cord and trigeminal nucleus caudalis J Comp Neurol 356 1995 327 344
15. D.M. Cain, S.G. Khasabov, and D.A. Simone Response properties of mechanoreceptors and nociceptors in mouse glabrous skin: an in vivo study J Neurophysiol 85 2001 1561 1574
16. N.M. Carmichael, J.O. Dostrovsky, and M.P. Charlton Peptide-mediated transdermal delivery of botulinum neurotoxin type A reduces neurogenic inflammation in the skin PAIN® 149 2010 316 324
17. M.J. Caterina, M.A. Schumacher, M. Tominaga, T.A. Rosen, J.D. Levine, and D. Julius The capsaicin receptor: a heat-activated ion channel in the pain pathway Nature 389 1997 816 824
18. S.R. Chaplan, A.B. Malmberg, and T.L. Yaksh Efficacy of spinal NMDA receptor antagonism in formalin hyperalgesia and nerve injury evoked allodynia in the rat J Pharmacol Exp Ther 280 1997 829 838
19. R.E. Coggeshall Fos, nociception and the dorsal horn Prog Neurobiol 77 2005 299 352
20. M. Cui, S. Khanijou, J. Rubino, and K.R. Aoki Subcutaneous administration of botulinum toxin A reduces formalin-induced pain PAIN® 107 2004 125 133
21. T.C. De Rojas, and B.D. Goldstein Lack of evidence for the size principle of selective vulnerability of axons in toxic neuropathies. I. The effects of subcutaneous injections of 2,5-hexanedione on behavior and muscle spindle function Toxicol Appl Pharmacol 104 1990 47 58
22. H.C. Diener, D.W. Dodick, S.K. Aurora, C.C. Turkel, R.E. DeGryse, R.B. Lipton, S.D. Silberstein, and M.F. Brin OnabotulinumtoxinA for treatment of chronic migraine: results from the double-blind, randomized, placebo-controlled phase of the PREEMPT 2 trial Cephalalgia 30 2010 804 814
23. D.M. Dirig, A. Salami, M.L. Rathbun, G.T. Ozaki, and T.L. Yaksh Characterization of variables defining hindpaw withdrawal latency evoked by radiant thermal stimuli J Neurosci Methods 76 1997 183 191
24. D.W. Dodick, C.C. Turkel, R.E. DeGryse, S.K. Aurora, S.D. Silberstein, R.B. Lipton, H.C. Diener, and M.F. Brin OnabotulinumtoxinA for treatment of chronic migraine: pooled results from the double-blind, randomized, placebo-controlled phases of the PREEMPT clinical program Headache 50 2010 921 936
25. J.O. Dolly, and M.A. O'Connell Neurotherapeutics to inhibit exocytosis from sensory neurons for the control of chronic pain Curr Opin Pharmacol 12 2012 100 108
26. J.O. Dolly, J. Wang, T.H. Zurawski, and J. Meng Novel therapeutics based on recombinant botulinum neurotoxins to normalize the release of transmitters and pain mediators FEBS J 278 2011 4454 4466
27. J.M. Donatelle Growth of the corticospinal tract and the development of placing reactions in the postnatal rat J Comp Neurol 175 1977 207 231
28. V. Drinovac, L. Bach-Rojecky, I. Matak, and Z. Lacković Involvement of μ-opioid receptors in antinociceptive action of botulinum toxin type A Neuropharmacology 70 2013 331 337
29. L.A. Elferink, W.S. Trimble, and R.H. Scheller Two vesicle-associated membrane protein genes are differentially expressed in the rat central nervous system J Biol Chem 264 1989 11061 11064
30. G. Fabregat, J.M. Asensio-Samper, S. Palmisani, V.L. Villanueva-Perez, and J. De Andres Subcutaneous botulinum toxin for chronic post-thoracotomy pain Pain Pract 13 2013 231 234
31. L. Foster, L. Clapp, M. Erickson, and B. Jabbari Botulinum toxin A and chronic low back pain: a randomized, double-blind study Neurology 56 2001 1290 1293
32. R. Gamse, and A. Saria Potentiation of tachykinin-induced plasma protein extravasation by calcitonin gene-related peptide Eur J Pharmacol 114 1985 61 66
33. P. Gazerani, N.S. Pedersen, A.M. Drewes, and L. Arendt-Nielsen Botulinum toxin type A reduces histamine-induced itch and vasomotor responses in human skin Br J Dermatol 161 2009 737 745
34. P. Gazerani, N.S. Pedersen, C. Staahl, A.M. Drewes, and L. Arendt-Nielsen Subcutaneous Botulinum toxin type A reduces capsaicin-induced trigeminal pain and vasomotor reactions in human skin PAIN® 141 2009 60 69
35. P. Geppetti, R. Nassini, S. Materazzi, and S. Benemei The concept of neurogenic inflammation BJU Int 101 2008 2 6
36. E.L. Hoschouer, D.M. Basso, and L.B. Jakeman Aberrant sensory responses are dependent on lesion severity after spinal cord contusion injury in mice PAIN® 148 2010 328 342
37. X.Y. Hua, P. Chen, E. Polgar, I. Nagy, M. Marsala, E. Phillips, L. Wollaston, L. Urban, T.L. Yaksh, and M. Webb Spinal neurokinin NK1 receptor down-regulation and antinociception: effects of spinal NK1 receptor antisense oligonucleotides and NK1 receptor occupancy J Neurochem 70 1998 688 698
38. P.P. Huang, I. Khan, M.S. Suhail, S. Malkmus, and T.L. Yaksh Spinal botulinum neurotoxin B: effects on afferent transmitter release and nociceptive processing PLoS One 6 2011 e19126
39. C.R. Huete, and P.E. Bermejo Botulinum toxin type A in the treatment of neuropathic pain in a case of postherpetic neuralgia Neurologia 23 2008 259 262
40. Y. Humeau, F. Doussau, N.J. Grant, and B. Poulain How botulinum and tetanus neurotoxins block neurotransmitter release Biochimie 82 2000 427 446
41. J.L. Hylden, and G.L. Wilcox Intrathecal substance P elicits a caudally-directed biting and scratching behavior in mice Brain Res 217 1981 212 215
42. K. Jhamandas, T.L. Yaksh, G. Harty, J. Szolcsanyi, and V.L. Go Action of intrathecal capsaicin and its structural analogues on the content and release of spinal substance P: selectivity of action and relationship to analgesia Brain Res 306 1984 215 225
43. D. Julius, and A.I. Basbaum Molecular mechanisms of nociception Nature 413 2001 203 210
44. I. Kangra, J.S.A. Lareau, and M. Randic The effect of substance P and calcitonin-gene-related peptide on the efflux of endogenous glutamate and aspartate from the rat spinal dorsal horn in vitro Neurosci Lett 108 1990 155 160
45. I. Kangra, and M. Randlt Tachykinin and calcitonin gene related peptide enhance release of endogenous glutamate and aspartate from the rat spinal dorsal horn slice Neuroscience 10 1990 2026 2038
46. R. Kawagoe, K. Onodera, and A. Takeuchi The release of endogenous glutamate from the newborn rat spinal cord induced by dorsal root stimulation and substance P Biomed Res 7 1986 253 259
47. U. Kern, M. Kohl, U. Seifert, and T. Schlereth Botulinum toxin type B in the treatment of residual limb hyperhidrosis for lower limb amputees: a pilot study Am J Phys Med Rehabil 90 2011 321 329
48. I. Kondo, J.C. Marvizon, B. Song, F. Salgado, S. Codeluppi, X.Y. Hua, and T.L. Yaksh Inhibition by spinal mu- and delta-opioid agonists of afferent-evoked substance P release J Neurosci 25 2005 3651 3660
49. H.H. Kramer, C. Angerer, F. Erbguth, M. Schmelz, and F. Birklein Botulinum Toxin A reduces neurogenic flare but has almost no effect on pain and hyperalgesia in human skin J Neurol 250 2003 188 193
50. G. Lalli, S. Bohnert, K. Deinhardt, C. Verastegui, and G. Schiavo The journey of tetanus and botulinum neurotoxins in neurons Trends Microbiol 11 2003 431 437
51. G.W. Lawrence, S.V. Ovsepian, J.F. Wang, K.R. Aoki, and J.O. Dolly Extravesicular intraneuronal migration of internalized botulinum neurotoxins without detectable inhibition of distal neurotransmission Biochem J 441 2012 443 452
52. I.J. Lever, A.D. Grant, S. Pezet, N.P. Gerard, S.D. Brain, and M. Malcangio Basal and activity-induced release of substance P from primary afferent fibres in NK1 receptor knockout mice: evidence for negative feedback Neuropharmacology 45 2003 1101 1110
53. H.S. Li, and Z.Q. Zhao Small sensory neurons in the rat dorsal root ganglia express functional NK-1 tachykinin receptor Eur J Neurosci 10 1998 1292 1299
54. N.K. Littlewood, A.J. Todd, R.C. Spike, C. Watt, and S.A.S. Shehab The types of neuron in spinal dorsal horn which possess neurokinin-1 receptors Neuroscience 66 1995 597 608
55. H.T. Liu, S.K. Tsai, M.C. Kao, and J.S. Hu Botulinum toxin A relieved neuropathic pain in a case of post-herpetic neuralgia Pain Med 7 2006 89 91
56. S. Luvisetto, S. Marinelli, S. Cobianchi, and F. Pavone Anti-allodynic efficacy of botulinum neurotoxin A in a model of neuropathic pain Neuroscience 145 2007 1 4
57. S. Luvisetto, S. Marinelli, F. Lucchetti, F. Marchi, S. Cobianchi, O. Rossetto, C. Montecucco, and F. Pavone Botulinum neurotoxins and formalin-induced pain: central vs. peripheral effects in mice Brain Res 1082 2006 124 131
58. B. Lynn, W. Ye, and B. Cotsell The actions of capsaicin applied topically to the skin of the rat on C-fiber afferents, antidromic vasodilation and substance P levels Br J Pharmacol 107 1992 400 406
59. L. Ma, J. Nagai, Y. Sekino, Y. Goto, S. Nakahira, and H. Ueda Single application of A2 NTX, a botulinum toxin A2 subunit, prevents chronic pain over long periods in both diabetic and spinal cord injury-induced neuropathic pain models J Pharmacol Sci 119 2012 282 286
60. V. Maienschein, M. Marxen, W. Volknandt, and H. Zimmermann A plethora of presynaptic proteins associated with ATP-storing organelles in cultured astrocytes Glia 26 1999 233 244
61. M. Malcangio, and N.G. Bowery Effect of the tachykinin NK1 receptor antagonists, RP 67580 and SR 140333, on electrically-evoked substance P release from rat spinal cord Br J Pharmacol 113 1994 635 641
62. S. Malkmus, X. Lu, T. Bartfai, T.L. Yaksh, and X.Y. Hua Increased hyperalgesia after tissue injury and faster recovery of allodynia after nerve injury in the GalR1 knockout mice Neuropeptides 39 2005 217 221
63. A.B. Malmberg, and T.L. Yaksh Hyperalgesia mediated by spinal glutamate or substance P receptor blocked by spinal cyclooxygenase inhibition Science 257 1992 1276 1279
64. P.W. Mantyh, S.D. Rogers, P. Honore, B.J. Allen, J.R. Ghilardi, J. Li, R.S. Daughters, D.A. Lappi, R.G. Wiley, and D.A. Simone Inhibition of hyperalgesia by ablation of lamina I spinal neurones expressing the substance P receptor Science 278 1997 275 279
65. V. Marchand-Pauvert, C. Aymard, L.S. Giboin, F. Dominici, A. Rossi, and R. Mazzocchio Beyond muscular effects: depression of spinal recurrent inhibition after botulinum neurotoxin A J Physiol 591 2013 1017 1029
66. S. Marinelli, S. Luvisetto, S. Cobianchi, W. Makuch, I. Obara, E. Mezzaroma, M. Caruso, E. Straface, B. Przewlocka, and F. Pavone Botulinum neurotoxin type A counteracts neuropathic pain and facilitates functional recovery after peripheral nerve injury in animal models Neuroscience 171 2010 316 328
67. S. Marinelli, V. Vacca, R. Ricordy, C. Uggenti, A.M. Tata, S. Luvisetto, and F. Pavone The analgesic effect on neuropathic pain of retrogradely transported botulinum neurotoxin A involves Schwann cells and astrocytes PLoS One 7 2012 e47977
68. J.C.G. Marvizon, X. Wang, Y. Matsuka, J.K. Neubert, and I. Spigelman Relationship between capsaicin-evoked substance P release and neurokinin 1 receptor internalization in the rat spinal cord Neuroscience 118 2003 535 545
69. I. Matak, L. Bach-Rojecky, B. Filipovic, and Z. Lackovic Behavioral and immunohistochemical evidence for central antinociceptive activity of botulinum toxin A Neuroscience 186 2011 201 207
70. I. Matak, P. Riederer, and Z. Lackovic Botulinum toxin's axonal transport from periphery to the spinal cord Neurochem Int 61 2012 236 239
71. I. Matak, I. Stracenski, and Z. Lackovic Comparison of analgesic effects of single versus repeated injection of botulinum toxin in orofacial formalin test in rats J Neural Transm 120 2013 141 144
72. D.M. McDonald, J.J. Bowden, P. Baluk, and N.W. Bunnett Neurogenic inflammation. A model for studying efferent actions of sensory nerves Adv Exp Med Biol 410 1996 453 462
73. C.R. McNamara, J. Mandel-Brehm, D.M. Bautista, J. Siemens, K.L. Deranian, M. Zhao, N.J. Hayward, J.A. Chong, D. Julius, M.M. Moran, and C.M. Fanger TRPA1 mediates formalin-induced pain Proc Natl Acad Sci U S A 104 2007 13525 13530
74. J.H. Meng, J.F. Wang, G. Lawrence, and J.O. Dolly Synaptobrevin I mediates exocytosis of CGRP from sensory neurons and inhibition by botulinum toxins reflects their anti-nociceptive potential J Cell Sci 120 2007 2864 2874
75. C. Montecucco, and J. Molgo Botulinal neurotoxins: revival of an old killer Curr Opin Pharmacol 5 2005 274 279
76. A. Nazarian, G. Gu, N.G. Gracias, K. Wilkinson, X.Y. Hua, M.R. Vasko, and T.L. Yaksh Spinal N-methyl-d-aspartate receptors and nociception-evoked release of primary afferent substance P Neuroscience 152 2008 119 127
77. M.L. Nichols, B.J. Allen, S.D. Rogers, J.R. Ghilardi, P. Honore, N.M. Luger, M.P. Finke, J. Li, D.A. Lappi, D.A. Simone, and P.W. Mantyh Transmission of nociception by spinal neurones expressing the substance P receptor Science 286 1999 1558 1561
78. M. Numazaki, and M. Tominaga Nociception and TRP channels Curr Drug Targets CNS Neurol Disord 3 2004 479 485
79. H.J. Park, Y. Lee, J. Lee, C. Park, and D.E. Moon The effects of botulinum toxin A on mechanical and cold allodynia in a rat model of neuropathic pain Can J Anaesth 53 2006 470 477
80. S.C. Pingle, J.A. Matta, and G.P. Ahern Capsaicin receptor: TRPV1 a promiscuous TRP channel Handb Exp Pharmacol 2007 155 171
81. E.J. Piovesan, H.G. Teive, P.A. Kowacs, M.V. Della Coletta, L.C. Werneck, and S.D. Silberstein An open study of botulinum-A toxin treatment of trigeminal neuralgia Neurology 65 2005 1306 1308
82. J. Purkiss, M. Welch, S. Doward, and K. Foster Capsaicin-stimulated release of substance P from cultured dorsal root ganglion neurons: involvement of two distinct mechanisms Biochem Pharmacol 59 2000 1403 1406
83. D. Ranoux, N. Attal, F. Morain, and D. Bouhassira Botulinum toxin type A induces direct analgesic effects in chronic neuropathic pain Ann Neurol 64 2008 274 283
84. L. Restani, F. Antonucci, L. Gianfranceschi, C. Rossi, O. Rossetto, and M. Caleo Evidence for anterograde transport and transcytosis of botulinum neurotoxin A (BoNT/A) J Neurosci 31 2011 15650 15659
85. L. Restani, F. Giribaldi, M. Manich, K. Bercsenyi, G. Menendez, O. Rossetto, M. Caleo, and G. Schiavo Botulinum neurotoxins A and E undergo retrograde axonal transport in primary motor neurons PLoS Pathog 8 2012 e1003087
86. L. Restani, E. Novelli, D. Bottari, P. Leone, I. Barone, L. Galli-Resta, E. Strettoi, and M. Caleo Botulinum neurotoxin A impairs neurotransmission following retrograde transynaptic transport Traffic 13 2012 1083 1089
87. G. Schiavo, F. Benfenati, B. Poulain, O. Rossetto, P. Polverino de Laureto, B.R. DasGupta, and C. Montecucco Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin Nature 359 1992 832 835
88. G. Schiavo, M. Matteoli, and C. Montecucco Neurotoxins affecting neuroexocytosis Physiol Rev 80 2000 717 766
89. W.J. Schulte-Mattler, O. Opatz, W. Blersch, A. May, H. Bigalke, and K. Wohlfahrt Botulinum toxin A does not alter capsaicin-induced pain perception in human skin J Neurol Sci 260 2007 38 42
90. L. Simpson The life history of a botulinum toxin molecule Toxicon 68 2013 40 59
91. U. Slawinska, H. Majczynski, Y. Dai, and L.M. Jordan The upright posture improves plantar stepping and alters responses to serotonergic drugs in spinal rats J Physiol 590 2012 1721 1736
92. T. Takasusuki, and T.L. Yaksh Regulation of spinal substance p release by intrathecal calcium channel blockade Anesthesiology 115 2011 153 164
93. Y.X. Tao, F. Wei, and Z.Q. Zhao A contribution of neurokinin-1 receptor to formalin-induced cFos expression in the rat spinal dorsal horn Neurosci Lett 221 1997 105 108
94. D. Tarsy, and E.R. First Painful cervical dystonia: clinical features and response to treatment with botulinum toxin Mov Disord 14 1999 1043 1045
95. A.J. Todd Anatomy of primary afferents and projection neurones in the rat spinal dorsal horn with particular emphasis on substance P and the neurokinin 1 receptor Exp Physiol 87 2002 245 249
96. Y. Torii, N. Akaike, T. Harakawa, K. Kato, N. Sugimoto, Y. Goto, S. Nakahira, T. Kohda, S. Kozaki, R. Kaji, and A. Ginnaga Type A1 but not type A2 botulinum toxin decreases the grip strength of the contralateral foreleg through axonal transport from the toxin-treated foreleg of rats J Pharm Sci 117 2011 275 285
97. W.S. Trimble, T.S. Gray, L.A. Elferink, M.C. Wilson, and R.H. Scheller Distinct patterns of expression of two VAMP genes within the rat brain J Neurosci 10 1990 1380 1387
98. V. Tugnoli, J.G. Capone, R. Eleopra, R. Quatrale, M. Sensi, E. Gastaldo, M.R. Tola, and P. Geppetti Botulinum toxin type A reduces capsaicin-evoked pain and neurogenic vasodilatation in human skin PAIN® 130 2007 76 83
99. A. Tzabazis, M. Klyukinov, N. Manering, M.I. Nemenov, S.L. Shafer, and D.C. Yeomans Differential activation of trigeminal C or Adelta nociceptors by infrared diode laser in rats: behavioral evidence Brain Res 1037 2005 148 156
100. V. Vacca, S. Marinelli, S. Luvisetto, and F. Pavone Botulinum toxin A increases analgesic effects of morphine, counters development of morphine tolerance and modulates glia activation and μ opioid receptor expression in neuropathic mice Brain Behav Immun 32 2013 40 50
101. B. Voller, T. Sycha, B. Gustorff, L. Schmetterer, S. Lehr, H.G. Eichler, E. Auff, and P. Schnider A randomized, double-blind, placebo controlled study on analgesic effects of botulinum toxin A Neurology 61 2003 940 944
102. G.S. von Banchet, and H.G. Schaible Localization of the neurokinin 1 receptor on a subset of substance P-positive and isolectin B4-negative dorsal root ganglion neurons of the rat Neurosci Lett 274 1999 175 178
103. L. Xiao, J. Cheng, Y. Zhuang, W. Qu, J. Muir, H. Liang, and D. Zhang Botulinum toxin type A reduces hyperalgesia and TRPV1 expression in rats with neuropathic pain Pain Med 14 2013 276 286
104. L. Xiao, S. Mackey, H. Hui, D. Xong, Q. Zhang, and D. Zhang Subcutaneous injection of botulinum toxin a is beneficial in postherpetic neuralgia Pain Med 11 2010 1827 1833
105. T.L. Yaksh, T.M. Jessell, R. Gamse, A.W. Mudge, and S.E. Leeman Intrathecal morphine inhibits substance P release from mammalian spinal cord in vivo Nature 286 1980 155 157
106. T.L. Yaksh, G. Ozaki, D. McCumber, M. Rathbun, C. Svensson, S. Malkmus, and M.C. Yaksh An automated flinch detecting system for use in the formalin nociceptive bioassay J Appl Physiol 90 2001 2386 2402
107. T. Yamamoto, and T.L. Yaksh Stereospecific effects of a nonpeptidic NK1 selective antagonist, CP-96,345: antinociception in the absence of motor dysfunction Life Sci 49 1991 1955 1963
108. R.Y. Yuan, J.J. Sheu, J.M. Yu, W.T. Chen, I.J. Tseng, H.H. Chang, and C.J. Hu Botulinum toxin for diabetic neuropathic pain: a randomized double-blind crossover trial Neurology 72 2009 1473 1478
109. X. Zhang, C. Pietra, E. Lovati, and W.C. de Groat Activation of neurokinin-1 receptors increases the excitability of guinea pig dorsal root ganglion cells J Pharmacol Exp Ther 343 2012 44 52