Differential pharmacological alleviation of oxaliplatin-induced hyperalgesia/allodynia at cephalic versus extra-cephalic level in rodents

Neuropharmacology

Volumn 79, Issue , 2014, Pages 432-443

  Michot, Benoit ^a   Kayser, Valérie ^a   Bastian, Gérard ^b   Bourgoin, Sylvie ^a   Hamon, Michel ^a  

^a INSERM   (France)

^b SORBONNE UNIVERSITÉ   (France)

Author keywords

Cold hyperalgesia; Inflammatory pain; Mechanical allodynia; Neuropathic pain; Oxaliplatin; Rodents

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; ACETONE; FORMALDEHYDE; GABAPENTIN; MORPHINE; NARATRIPTAN; OLCEGEPANT; OXALIPLATIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; 4 AMINOBUTYRIC ACID; AMINE; ANALGESIC AGENT; CYCLOHEXANECARBOXYLIC ACID DERIVATIVE; DIPEPTIDE; PIPERIDINE DERIVATIVE; PLATINUM COMPLEX; QUINAZOLINE DERIVATIVE; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; TRPA1 PROTEIN, RAT; TRYPTAMINE DERIVATIVE;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; COLD STRESS; CONTROLLED STUDY; DRUG EFFICACY; HYPERALGESIA; MALE; MECHANICAL STRESS; MOUSE; NERVE CELL; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STIMULUS RESPONSE; UPREGULATION; VIBRISSA; VON FREY TEST; ANIMAL; C57BL MOUSE; COLD; DRUG EFFECTS; METABOLISM; PATHOPHYSIOLOGY; SPINAL CORD; SPINAL GANGLION; SPRAGUE DAWLEY RAT; TOUCH;

8-HYDROXY-2-(DI-N-PROPYLAMINO)TETRALIN; AMINES; ANALGESICS; ANIMALS; COLD TEMPERATURE; CYCLOHEXANECARBOXYLIC ACIDS; DIPEPTIDES; FORMALDEHYDE; GAMMA-AMINOBUTYRIC ACID; GANGLIA, SPINAL; HYPERALGESIA; MALE; MICE; MICE, INBRED C57BL; MORPHINE; ORGANOPLATINUM COMPOUNDS; PIPERIDINES; QUINAZOLINES; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; TOUCH; TRPC CATION CHANNELS; TRYPTAMINES;

EID: 84891823695     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.12.011     Document Type: Article

References (74)

1. F.V. Abbott, R. Ocvirk, R. Najafee, and K.B. Franklin Improving the efficiency of the formalin test Pain 83 1999 561 569
2. 3 receptor expression differs from dorsal root ganglion and is modulated by deep tissue inflammation Pain 117 2005 280 291 (Pubitemid 41383524)
3. N. Attal, G. Cruccu, R. Baron, M. Haanpää, P. Hansson, T.S. Jensen, T. Nurmikko, and Eur Fed Neurol Soc EFNS guidelines on the pharmacological treatment of neuropathic pain: 2010 revision Eur. J. Neurol. 17 2010 1113-e88
4. D. Balayssac, J. Ferrier, J. Descoeur, B. Ling, D. Pezet, A. Eschalier, and N. Authier Chemotherapy-induced peripheral neuropathies: from clinical relevance to preclinical evidence Expert Opin. Drug Saf. 10 2011 407 417
5. 1A receptor-mediated, behaviorally specific analgesia Eur. J. Pharmacol. 421 2001 109 114 (Pubitemid 32524081)
6. R. Baron, A. Binder, and G. Wasner Neuropathic pain: diagnosis, pathophysiological mechanisms, and treatment Lancet Neurol. 9 2010 807 819
7. A.I. Basbaum, D.M. Bautista, G. Scherrer, and D. Julius Cellular and molecular mechanisms of pain Cell 139 2009 267 284
8. E.E. Benarroch Central neuron-glia interactions and neuropathic pain: overview of recent concepts and clinical implications Neurology 75 2010 273 278
9. + channels in frog peripheral myelinated axons Gen. Physiol. Biophys. 25 2006 263 276 (Pubitemid 44857440)
10. R. Benoliel, E. Eliav, and M. Tal No sympathetic nerve sprouting in rat trigeminal ganglion following painful and non-painful infraorbital nerve neuropathy Neurosci. Lett. 297 2001 151 154 (Pubitemid 32011296)
11. J.V. Berger, L. Knaepen, S.P.M. Janssen, R.J.P. Jaken, M.A.E. Marcus, E.A.J. Joosten, and R. Deumens Cellular and molecular insights into neuropathy-induced pain hypersensitivity for mechanism-based treatment approaches Brain Res. Rev. 67 2011 282 310
12. G. Cavaletti, G. Tredici, M.G. Petruccioli, E. Donde, P. Tredici, P. Marmiroli, C. Minoia, A. Ronchi, M. Bayssas, and G.G. Etienne Effects of different schedules of oxaliplatin treatment on the peripheral nervous system of the rat Eur. J. Cancer 37 2001 2457 2463 (Pubitemid 33097486)
13. D. Christensen, M. Gautron, G. Guilbaud, and V. Kayser Effect of gabapentin and lamotrigine on mechanical allodynia-like behaviour in a rat model of trigeminal neuropathic pain Pain 93 2001 147 153 (Pubitemid 32568400)
14. H.E. Connor, W. Feniuk, D.T. Beattie, P.C. North, A.W. Oxford, D.A. Saynor, and P.P. Humphrey Naratriptan: biological profile in animal models relevant to migraine Cephalalgia 17 1997 145 152 (Pubitemid 27257338)
15. L. Davoody, R.L. Quiton, J.M. Lucas, Y. Ji, A. Keller, and R. Masri Conditioned place preference reveals tonic pain in an animal model of central pain J. Pain 12 2011 868 874
16. J. Descoeur, V. Pereira, A. Pizzoccaro, A. François, B. Ling, V. Maffre, B. Couette, J. Busserolles, C. Courteix, J. Noël, M. Lazdunski, A. Eschalier, N. Authier, and E. Bourinet Oxaliplatin-induced cold hypersensitivity is due to remodelling of ion channel expression in nociceptors EMBO Mol. Med. 3 2011 266 278
17. H. Doods, K. Arndt, K. Rudolf, and S. Just CGRP antagonists: unraveling the role of CGRP in migraine Trends Pharmacol. Sci. 28 2007 580 587 (Pubitemid 350026615)
18. L. Edvinsson, and T.W. Ho CGRP receptor antagonism and migraine Neurotherapeutics 7 2010 164 175
19. J.M. Extra, M. Marty, S. Brienza, and J.L. Misset Pharmacokinetics and safety profile of oxaliplatin Semin. Oncol. 25 1998 13 22 (Pubitemid 28248697)
20. M.J. Fischer, S. Koulchitsky, and K. Messlinger The nonpeptide calcitonin gene-related peptide receptor antagonist BIBN4096BS lowers the activity of neurons with meningeal input in the rat spinal trigeminal nucleus J. Neurosci. 25 2005 5877 5883 (Pubitemid 40911418)
21. K. Fried, U. Bongenhielm, F.M. Boissonade, and P.P. Robinson Nerve injury-induced pain in the trigeminal system The Neuroscientist 7 2001 155 165 (Pubitemid 32245021)
22. P. Gauchan, T. Andoh, A. Kato, and Y. Kuraishi Involvement of increased expression of transient receptor potential melastatin 8 in oxaliplatin-induced cold allodynia in mice Neurosci. Lett. 458 2009 93 95
23. P.J. Goadsby, and J.D. Classey Evidence for serotonin (5-HT)1B, 5-HT1D and 5-HT1F receptor inhibitory effects on trigeminal neurons with craniovascular input Neuroscience 12 2003 491 498 (Pubitemid 37419958)
24. 1B/1D) receptors Br. J. Pharmacol. 122 1997 918 922 (Pubitemid 27460175)
25. M.A. Graham, G.F. Lockwood, D. Greenslade, S. Brienza, M. Bayssas, and E. Gamelin Clinical pharmacokinetics of oxaliplatin: a critical review Clin. Cancer. Res. 6 2000 1205 1218 (Pubitemid 30226200)
26. F. Grolleau, L. Gamelin, M. Boisdron-Celle, B. Lapied, M. Pelhate, and E. Gamelin A possible explanation for a neurotoxic effect of the anticancer agent oxaliplatin on neuronal voltage-gated sodium channels J. Neurophysiol. 85 2001 2293 2297 (Pubitemid 32440704)
27. G. Guilbaud, M. Gautron, F. Jazat, H. Ratinahirana, R. Hassig, and J.J. Hauw Time course of degeneration and regeneration of myelinated nerve fibres following chronic loose ligatures of the rat sciatic nerve: can nerve lesions be linked to the abnormal pain-related behaviours? Pain 53 1993 147 158 (Pubitemid 23161576)
28. K.M. Hargreaves Orofacial pain Pain 152 2011 S25 S32
29. P. Honoré, P. Chandran, G. Hernandez, D.M. Gauvin, J.P. Mikusa, C. Zhong, S.K. Joshi, J.R. Ghilardi, M.A. Sevcik, R.M. Fryer, J.A. Segreti, P.N. Banfor, K. Marsh, T. Neelands, E. Bayburt, J.F. Daanen, A. Gomtsyan, C.H. Lee, M.E. Kort, R.M. Reilly, C.S. Surowy, P.R. Kym, P.W. Mantyh, J.P. Sullivan, M.F. Jarvis, and C.R. Faltynek Repeated dosing of ABT-102, a potent and selective TRPV1 antagonist, enhances TRPV1-mediated analgesic activity in rodents, but attenuates antagonist-induced hyperthermia Pain 142 2009 27 35
30. J.J. Idanpaan-Heikkila, and G. Guilbaud Pharmacological studies on a rat model of trigeminal neuropathic pain: baclofen, but not carbamazepine, morphine or tricyclic antidepressants, attenuates the allodynia-like behaviour Pain 79 1999 281 290 (Pubitemid 29076763)
31. K. Inoue, and M. Tsuda Microglia and neuropathic pain Glia 57 2009 1469 1479
32. S.M. Jamieson, J. Liu, B. Connor, and M.J. McKeage Oxaliplatin causes selective atrophy of a subpopulation of dorsal root ganglion neurons without inducing cell loss Cancer Chemother. Pharmacol. 56 2005 391 399 (Pubitemid 41095402)
33. E.K. Joseph, and J.D. Levine Comparison of oxaliplatin- and cisplatin-induced painful peripheral neuropathy in the rat J. Pain 10 2009 534 541
34. 1B/1D receptor agonists, sumatriptan, zolmitriptan and dihydroergotamine, attenuate pain-related behaviour in a rat model of trigeminal neuropathic pain Br. J. Pharmacol. 137 2002 1287 1297 (Pubitemid 36071746)
35. V. Kayser, and D. Christensen Antinociceptive effect of systemic gabapentin in mononeuropathic rats, depends on stimulus characteristics and level of test integration Pain 88 2000 53 60
36. 3A-/- and 5-HTT-/- knock out male mice Pain 130 2007 235 248 (Pubitemid 46994702)
37. 1B/1D receptor stimulation in a rat model of trigeminal neuropathic pain Eur. J. Pain 15 2011 451 458
38. V. Kayser, F. Viguier, M. Ioannidi, J.F. Bernard, A. Latremoliere, B. Michot, J.M. Vela, H. Buschmann, M. Hamon, and S. Bourgoin Differential anti-neuropathic pain effects of tetrodotoxin in sciatic nerve- versus infraorbital nerve-ligated rats-Behavioral, pharmacological and immunohistochemical investigations Neuropharmacology 58 2010 474 487
39. K.J. Kim, Y.W. Yoon, and J.M. Chung Comparison of three rodent neuropathic pain models Exp. Brain Res. 113 1997 200 206 (Pubitemid 27090842)
40. T. King, L. Vera-Portocarrero, T. Guttierez, T.W. Vanderah, G. Dussor, J. Lai, H.L. Fields, and F. Porreca Unmasking the tonic-aversive state in neuropathic pain Nat. Neurosci. 12 2009 1364 1366
41. A. Latrémolière, A. Mauborgne, J. Masson, S. Bourgoin, V. Kayser, M. Hamon, and M. Pohl Differential implication of proinflammatory cytokine interleukin-6 in the development of cephalic versus extracephalic neuropathic pain in rats J. Neurosci. 28 2008 8489 8501
42. G.D. Leonard, M.A. Wright, M.G. Quinn, S. Fioravanti, N. Harold, B. Schuler, R.R. Thomas, and J.L. Grem Survey of oxaliplatin-associated neurotoxicity using an interview-based questionnaire in patients with metastatic colorectal cancer BMC Cancer 5 2005 116
43. B. Ling, N. Authier, D. Balayssac, A. Eschalier, and F. Coudore Behavioral and pharmacological description of oxaliplatin-induced painful neuropathy in rat Pain 128 2007 225 234 (Pubitemid 46389544)
44. P. Luccarini, A. Childeric, A.M. Gaydier, D. Voisin, and R. Dallel The orofacial formalin test in the mouse: a behavioral model for studying physiology and modulation of trigeminal nociception J. Pain 7 2006 908 914 (Pubitemid 44854734)
45. W. Ma, and R. Quirion Increased calcitonin gene-related peptide in neuroma and invading macrophages is involved in the up-regulation of interleukin-6 and thermal hyperalgesia in a rat model of mononeuropathy J. Neurochem. 98 2006 180 192 (Pubitemid 43882943)
46. L. Meyer, C. Patte-Mensah, O. Taleb, and A.G. Mensah-Nyagan Allopregnanolone prevents and suppresses oxaliplatin-evoked painful neuropathy: multi-parametric assessment and direct evidence Pain 152 2011 170 181
47. B. Michot, S. Bourgoin, F. Viguier, M. Hamon, and V. Kayser Differential effects of calcitonin gene-related peptide receptor blockade by olcegepant on mechanical allodynia induced by ligation of the infraorbital nerve vs the sciatic nerve in the rat Pain 153 2012 1939 1948
48. R. Nassini, M. Gees, S. Harrison, G. De Siena, S. Materazzi, N. Moretto, P. Failli, D. Preti, N. Marchetti, A. Cavazzini, F. Mancini, P. Pedretti, B. Nilius, R. Patacchini, and P. Geppetti Oxaliplatin elicits mechanical and cold allodynia in rodents via TRPA1 receptor stimulation Pain 152 2011 1621 1631
49. E. Navratilova, J.Y. Xie, T. King, and F. Porreca Evaluation of reward from pain relief Ann. N. Y. Acad. Sci. 1282 2013 1 11
50. Y. Omori, K. Kagaya, R. Enomoto, A. Sasaki, T. Andoh, H. Nojima, H. Takahata, and Y. Kuraishi A mouse model of sural nerve injury-induced neuropathy: gabapentin inhibits pain-related behaviors and the hyperactivity of wide-dynamic range neurons in the dorsal horn J. Pharmacol. Sci. 109 2009 532 539
51. A. Ottani, E. Ferraris, D. Giuliani, C. Mioni, A. Bertolini, E. Sternieri, and A. Ferrari Effect of sumatriptan in different models of pain in rats Eur. J. Pharmacol. 497 2004 181 186 (Pubitemid 39092572)
52. S.B. Park, A.V. Krishnan, C.S. Lin, D. Goldstein, M. Friedlander, and M.C. Kiernan Mechanisms underlying chemotherapy-induced neurotoxicity and the potential for neuroprotective strategies Curr. Med. Chem. 15 2008 3081 3094
53. S.B. Park, C.S. Lin, A.V. Krishnan, D. Goldstein, M.L. Friedlander, and M.C. Kiernan Oxaliplatin-induced neurotoxicity: changes in axonal excitability precede development of neuropathy Brain 132 2009 2712 2723
54. L.M. Pasetto, M.R. D'Andrea, E. Rossi, and S. Monfardini Oxaliplatin-related neurotoxicity: how and why? Crit. Rev. Oncol. Hematol. 59 2006 159 168 (Pubitemid 44094106)
55. P.P. Robinson, F.M. Boissonade, A.R. Loescher, K.G. Smith, J.M. Yates, C. Elcock, E.V. Bird, S.L. Davies, P.L. Smith, and A.R. Vora Peripheral mechanisms for the initiation of pain following trigeminal nerve injury J. Orofac. Pain 18 2004 287 292 (Pubitemid 39531541)
56. J.H. Rosland, A. Tjølsen, B. Maehle, and K. Hole The formalin test in mice: effect of formalin concentration Pain 42 1990 235 242 (Pubitemid 20258908)
57. G. Saddi, and F.V. Abbott The formalin test in the mouse: a parametric analysis of scoring properties Pain 89 2000 53 63
58. M. Sakurai, N. Egashira, T. Kawashiri, T. Yano, H. Ikesue, and R. Oishi Oxaliplatin-induced neuropathy in the rat: involvement of oxalate in cold hyperalgesia but not mechanical allodynia Pain 147 2009 165 174
59. T.D. Schmittgen, and K.J. Livak Analyzing real-time PCR data by the comparative C(T) method Nat. Protoc. 3 2008 1101 1108 (Pubitemid 351818697)
60. M. Skingle, P.J. Birch, G.E. Leighton, and P.P. Humphrey Lack of antinociceptive activity of sumatriptan in rodents Cephalalgia 10 1990 207 212
61. S.B. Smith, S.E. Crager, and J.S. Mogil Paclitaxel-induced neuropathic hypersensitivity in mice: responses in 10 inbred mouse strains Life Sci. 74 2004 2593 2604 (Pubitemid 38369356)
62. V. Staikopoulos, B.J. Sessle, J.B. Furness, and E.A. Jennings Localization of P2X2 and P2X3 receptors in rat trigeminal ganglion neurons Neuroscience 144 2007 208 216 (Pubitemid 44839055)
63. L.E. Ta, A.J. Bieber, S.M. Carlton, C.L. Loprinzi, P.A. Low, and A.J. Windebank Transient receptor potential vanilloid 1 is essential for cisplatin-induced heat hyperalgesia in mice Mol. Pain 6 2010 15
64. L.E. Ta, P.A. Low, and A.J. Windebank Mice with cisplatin and oxaliplatin-induced painful neuropathy develop distinct early responses to thermal stimuli Mol. Pain 5 2009 9
65. 7 receptor activation in rats suffering from neuropathic pain Neuropharmacology 63 2012 1093 1106
66. A.J. Windebank, and W. Grisold Chemotherapy-induced neuropathy J. Periph. Nerv. Syst. 13 2008 27 46 (Pubitemid 351393018)
67. S. Wolf, D. Barton, L. Kottschade, A. Grothey, and C. Loprinzi Chemotherapy induced peripheral neuropathy: prevention and treatment strategies Eur. J. Cancer 44 2008 1507 1515
68. W.H. Xiao, H. Zheng, and G.J. Bennett Characterization of oxaliplatin-induced chronic painful peripheral neuropathy in the rat and comparison with the neuropathy induced by paclitaxel Neuroscience 203 2012 194 206
69. S.Y. Yoon, C.R. Robinson, H. Zhang, and P.M. Dougherty Spinal astrocyte gap junctions contribute to oxaliplatin-induced mechanical hypersensitivity J. Pain 14 2013 205 214
70. J.M. Zakrzewska Medical management of trigeminal neuropathic pains Expert Opin. Pharmacother. 11 2010 1239 1254
71. H. Zhang, S.Y. Yoon, and P.M. Dougherty Evidence that spinal astrocytes but not microglia contribute to the pathogenesis of paclitaxel-induced painful neuropathy J. Pain 13 2012 293 303
72. M. Zhao, K. Isami, S. Nakamura, H. Shirakawa, T. Nakagawa, and S. Kaneko Acute cold hypersensitivity characteristically induced by oxaliplatin is caused by the enhanced responsiveness of TRPA1 in mice Mol. Pain 8 2012 55
73. F.Y. Zheng, W.H. Xiao, and G.J. Bennett The response of spinal microglia to chemotherapy-evoked painful peripheral neuropathies is distinct from that evoked by traumatic nerve injuries Neuroscience 176 2011 447 454
74. M. Zimmermann Ethical guidelines for investigations of experimental pain in conscious animals Pain 16 1983 109 110 (Pubitemid 13058546)