Resiniferatoxin for pain treatment: An interventional approach to personalized pain medicine

Open Pain Journal

Volumn 6, Issue SPEC.ISSUE.1, 2013, Pages 95-107

  Iadarola, Michael J ^a,b   Gonnella, Gian Luigi ^a,c  

^a NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^b not available   (United States)

^c CATHOLIC UNIVERSITY   (Italy)

Author keywords

A delta fibers; Arachnoiditis; C fibers; Calcium cytotoxicity; Cancer pain; CGRP; Complex regional pain syndrome; Dog; Geriatric; Ion channel; Malignant pain; Neuropathic pain; Nonmalignant pain; Osteoarthritis; Osteosarcoma; Spinal stenosis; Substance P

Indexed keywords

ANTIDEPRESSANT AGENT; ANXIOLYTIC AGENT; CAPSAICIN; GABAPENTIN; LOCAL ANESTHETIC AGENT; NONSTEROID ANTIINFLAMMATORY AGENT; OPIATE; PARACETAMOL; PREGABALIN; RESINIFERATOXIN; STEROID; VANILLOID RECEPTOR 1;

A DELTA NERVE FIBER; ABLATION THERAPY; AMPUTATION; ANALGESIC ACTIVITY; ANTINOCICEPTION; BODY FLUID COMPARTMENT; BURN; C DELTA NERVE FIBER; CANCER SURGERY; CHRONIC PAIN; CORNEA DISEASE; CYSTITIS; DECOMPRESSION SURGERY; DELTA NERVE FIBER; DISEASE MODEL; DOSE RESPONSE; DRUG ADMINISTRATION ROUTE; DRUG EFFICACY; DRUG MECHANISM; DRUG RECEPTOR BINDING; DRUG SAFETY; DRUG TARGETING; EXPERIMENTAL DOG; EXPERIMENTAL RAT; HUMAN; LOW BACK PAIN; METATARSALGIA; NERVE INJURY; NEURALGIA; NEUROMA; NEUROPATHIC PAIN; NONHUMAN; OSTEOARTHRITIS; PAIN; PERINEURIUM; PERSONALIZED MEDICINE; POSTOPERATIVE PAIN; PRIORITY JOURNAL; QUALITY OF LIFE; REVIEW; VULVODYNIA;

EID: 84876089233     PISSN: None     EISSN: 18763863     Source Type: Journal    
DOI: 10.2174/1876386301306010095     Document Type: Review

References (94)

1. Huang SC, Korlipara VL. Neurokinin-1 receptor antagonists: a comprehensive patent survey. Expert Opin Ther Pat 2010; 20(8): 1019-45.
2. Stewart JM. Bradykinin antagonists: discovery and development. Peptides 2004; 25(3): 527-32.
3. Cannon GW, Breedveld FC efficacy of cyclooxygenase-2-specific inhibitors, Am J Med 2001; 110(Suppl 3A): 6S-12S.
4. Walpole CS, Bevan S, Bovermann G, et al. The discovery of capsazepine, the first competitive antagonist of the sensory neuron excitants capsaicin and resiniferatoxin. J Med Chem 1994; 37(13): 1942-54.
5. Patel L, Lindley C. Aprepitant--a novel NK1-receptor antagonist. Expert Opin Pharmacother 2003; 4(12): 2279-96.
6. Burnstock G. Do some nerve cells release more than one transmitter? Neuroscience 1976; 1(4): 239-48.
7. Hökfelt T, Arvidsson U, Cullheim S, et al. Multiple messengers in descending serotonin neurons: localization and functional implications. J Chem Neuroanat 2000; 18(1-2): 75-86.
8. Hnasko TS, Edwards RH. Neurotransmitter corelease: mechanism and physiological role. Annu Rev Physiol 2012; 74: 225-43.
9. Battaglia G, Rustioni A. Coexistence of glutamate and substance P in dorsal root ganglion neurons of the rat and monkey. J Comp Neurol 1988; 277(2): 302-12.
10. Mishra SK, Holzman S, Hoon MA. A nociceptive signaling role for neuromedin B J Neurosci 2012; 32(25): 8686-95.
11. Benyamin R, Trescot AM, Datta S, et al. Opioid complications and side effects. Pain Physician 2008; 11(2 Suppl): S105-20.
12. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997; 389: 816-24.
13. Jordt SE, McKemy DD, Julius D. Lessons from peppers and peppermint: the molecular logic of thermosensation. Curr Opin Neurobiol 2003; 13(4): 487-92.
14. Tominaga M, Caterina MJ. Thermosensation and pain. J Neurobiol 2004; 61(1): 3-12.
15. Moran MM, McAlexander MA, Bíró T, Szallasi A. Transient receptor potential channels as therapeutic targets. Nat Rev Drug Discov 2011; 10(8): 601-20.
16. Hardie RC. TRP channels and lipids: from Drosophila to mammalian physiology. J Physiol 2007; 578(Pt 1): 9-24.
17. Montell C. The history of TRP channels, a commentary and reflection. Pflugers Arch 2011; 461(5): 499-506.
18. Kort ME, Kym PR. TRPV1 antagonists: clinical setbacks and prospects for future development. Prog Med Chem 2012; 51: 57-70.
19. Waxman SG, Cummins TR, Dib-Hajj S, Fjell J, Black JA. Sodium channels, excitability of primary sensory neurons, and the molecular basis of pain. Muscle Nerve 1999; 22(9): 1177-87.
20. Akopian AN, Sivilotti L, Wood JN. A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 1996; 379(6562): 257-62.
21. Lane NE, Schnitzer TJ, Birbara CA, Mokhtarani, et al. Tanezumab for the treatment of pain from osteoarthritis of the knee. N Engl J Med 2010; 363(16): 1521-31.
22. Dubovy P. Wallerian degeneration and peripheral nerve conditions for both axonal regeneration and neuropathic pain induction. Ann Anat 2011; 193: 267-75.
23. Taveggia C, Feltri ML, Wrabetz L. Signals to promote myelin formation and repair. Nat Rev Neurol 2010; 6(5): 276-87.
24. Ma Q. Labeled lines meet and talk: population coding of somatic sensations. J Clin Invest 2010; 120(11): 3773-8.
25. Brown MT, Murphy FT, Radin DM, Davignon I, Smith MD, West CR. Tanezumab Reduces Osteoarthritic Knee Pain: results of a Tandomized, Double-Blind, Placebo-Controlled Phase III Trial. J Pain 2012; 13(8): 790-8.
26. Garber K. Fate of novel painkiller mAbs hangs in balance. Nat Biotechnol 2011; 29 (3): 173-4.
27. Rowbotham MC, Nothaft W, Duan WR, et al. Oral and cutaneous thermosensory profile of selective TRPV1 inhibition by ABT-102 in a randomized healthy volunteer trial. Pain 2011; 152(5): 1192-200.
28. Gavva NR, Treanor JJ, Garami A, et al. Pharmacological blockade of the vanilloid receptor TRPV1 elicits marked hyperthermia in humans. Pain 2008; 136(1-2): 202-10.
29. Wong GY, Gavva NR. Therapeutic potential of vanilloid receptor TRPV1 agonists and antagonists as analgesics: recent advances and setbacks. Brain Res Rev 2009; 60(1): 267-77.
30. Mannes AJ, Iadarola MJ. Complete pain relief: potential problems and diagnostic solutions. Nat Clin Pract Neurol 2007; 3(12): 648-9.
31. Mannes A, Iadarola M. Potential downsides of perfect pain relief. Nature 2007; 446 (7131): 24.
32. Vlassakov KV, Narang S, Kissin I. Local anesthetic blockade of peripheral nerves for treatment of neuralgias: systematic analysis. Anesth Analg 2011; 112(6): 1487-93.
33. McGee HT, Fraunfelder FW. Toxicities of topical ophthalmic anesthetics. Expert Opin Drug Saf 2007; 6: 637-40.
34. Bennett GJ. What is spontaneous pain and who has it? J Pain 2012; 13(10): 921-9.
35. Neubert JK, Karai L, Jun JH, Kim HS, Olah Z, Iadarola MJ. Peripherally induced resiniferatoxin analgesia. Pain 2003; 104(1-2): 219-28.
36. Kárai L, Brown DC, Mannes AJ, et al. Deletion of vanilloid receptor 1-expressing primary afferent neurons for pain control. J Clin Invest 2004; 113(9):1344-52.
37. Brown DC, Iadarola MJ, Perkowski SZ, et al. Physiologic and antinociceptive effects of intrathecal resiniferatoxin in a canine bone cancer model. Anesthesiology 2005; 103(5): 1052-9.
38. Bates BD, Mitchell K, Keller JM, et al. Prolonged analgesic response of cornea to topical resiniferatoxin, a potent TRPV1 agonist. Pain 2010; 149(3): 522-8.
39. Kissin I, Bright CA, Bradley EL Jr. Selective and long-lasting neural blockade with resiniferatoxin prevents inflammatory pain hypersensitivity. Anesth Analg 2002; 94(5): 1253-8.
40. Kissin I, Freitas CF, Mulhern HL, DeGirolami U. Sciatic nerve block with resiniferatoxin: an electron microscopic study of unmyelinated fibers in the rat. Anesth Analg 2007; 105(3): 825-31.
41. Olah Z, Szabo T, Karai L, et al. Ligand-induced dynamic membrane changes and cell deletion conferred by vanilloid receptor 1. J Biol Chem 2001; 276(14): 11021-30.
42. Olah Z, Karai L, Iadarola MJ. Anandamide activates vanilloid receptor 1 (VR1) at acidic pH in dorsal root ganglia neurons and cells ectopically expressing VR1. J Biol Chem 2001; 276(33): 31163-70.
43. Gover TD, Moreira TH, Kao JP, Weinreich D. Calcium regulation in individual peripheral sensory nerve terminals of the rat. J Physiol 2007; 578(Pt 2): 481-90.
44. Gover TD, Moreira TH, Weinreich D. Role of calcium in regulating primary sensory neuronal excitability. Handb Exp Pharmacol 2009; (194): 563-87.
45. Hsieh YL, Chiang H, Tseng TJ, Hsieh ST. Enhancement of cutaneous nerve regeneration by 4-methylcatechol in resiniferatoxin-induced neuropathy. J Neuropathol Exp Neurol 2008; 67(2): 93-104.
46. Hsieh YL, Chiang H, Lue JH, Hsieh ST. P2X3-mediated peripheral sensitization of neuropathic pain in resiniferatoxin-induced neuropathy. Exp Neurol 2012; 235(1): 316-25.
47. Bishnoi M, Bosgraaf CA, Premkumar LS. Preservation of acute pain and efferent functions following intrathecal resiniferatoxininduced analgesia in rats. J Pain 2011; 12(9): 991-1003.
48. Mitchell K, Bates BD, Keller JM, et al. Ablation of rat TRPV1-expressing Adelta/C-fibers with resiniferatoxin: analysis of withdrawal behaviors, recovery of function and molecular correlates. Mol Pain 2010; 6: 94.
49. Yang HY, Mitchell K, Keller JM, Iadarola MJ. Peripheral inflammation increases Scya2 expression in sensory ganglia and cytokine and endothelial related gene expression in inflamed tissue. J Neurochem 2007; 103(4): 1628-43.
50. Wallace M, Pappagallo M. Qutenza®: a capsaicin 8% patch for the management of postherpetic neuralgia. Expert Rev Neurother 2011; 11(1): 15-27.
51. Simone DA, Nolano M, Johnson T, Wendelschafer-Crabb G, Kennedy WR. Intradermal injection of capsaicin in humans produces degeneration and subsequent reinnervation of epidermal nerve fibers: correlation with sensory function. J Neurosci 1998; 18(21): 8947-59.
52. Iadarola MJ, Douglass J, Civelli O, Naranjo JR. Increased spinal cord dynorphin mRNA during peripheral inflammation. NIDA Res Monogr 1986; 75: 406-9.
53. Iadarola MJ, Douglass J, Civelli O, Naranjo JR. Differential activation of spinal cord dynorphin and enkephalin neurons during hyperalgesia: evidence using cDNA hybridization. Brain Res 1988; 455(2): 205-12.
54. Hollins M. Somesthetic senses. Annu Rev Psychol 2010; 61: 243-71.
55. Lopes C, Liu Z, Xu Y, Ma Q. Tlx3 and runx1 act in combination to coordinate the development of a cohort of nociceptors, thermoceptors, and pruriceptors. J Neurosci 2012; 32(28): 9706-15.
56. Mishra SK, Tisel SM, Orestes P, Bhangoo SK, Hoon MA. TRPV1-lineage neurons are required for thermal sensation. EMBO J 2011; 30(3): 582-93.
57. Marmigère F, Ernfors P. Specification and connectivity of neuronal subtypes in the sensory lineage. Nat Rev Neurosci 2007; 8(2): 114-27.
58. Li L, Rutlin M, Abraira VE, Cassidy C, et al. The functional organization of cutaneous low-threshold mechanosensory neurons. Cell 2011; 147(7): 1615-27.
59. Liu Y, Ma Q. Generation of somatic sensory neuron diversity and implications on sensory coding. Curr Opin Neurobiol 2011; 21(1): 52-60.
60. Franck MC, Stenqvist A, Li L, et al. Essential role of Ret for defining non-peptidergic nociceptor phenotypes and functions in the adult mouse. Eur J Neurosci 2011; 33(8): 1385-400.
61. Zylka MJ, Rice FL, Anderson DJ. Topographically distinct epidermal nociceptive circuits revealed by axonal tracers targeted to Mrgprd. Neuron 2005; 45(1): 17-25.
62. Ivanavicius SP, Blake DR, Chessell IP, Mapp PI. Isolectin B4 binding neurons are not present in the rat knee joint. Neuroscience 2004; 128(3): 555-60.
63. Cantillon M, Vause E, Sykes D, Tagoe M. Safety, tolerability and efficacy of intraoperative ALGRX 4975 in a randomized, doubleblind, placebo-controlled study of subjects undergoing bunionectomy. J Pain 2005; 6(3): S48.
64. Aasvang EK, Hansen JB, Malmstrøm J, et al. The effect of wound instillation of a novel purified capsaicin formulation on postherniotomy pain: a double-blind, randomized, placebocontrolled study. Anesth Analg 2008; 107(1): 282-91.
65. Kárai LJ, Russell JT, Iadarola MJ, Oláh Z. Vanilloid receptor 1 regulates multiple calcium compartments and contributes to Ca2+-induced Ca2+ release in sensory neurons. J Biol Chem 2004; 279(16): 16377-87.
66. Cantillon M, Vause E, Sykes D, Russell R, Moon A, Hughes S. Preliminary safety, tolerability and efficacy of ALGRX 4975 in osteoarthritis (OA) of the knee. J Pain 2005; 6(3): Suppl S39.
67. Apostolidis A, Gonzales GE, Fowler CJ. Effect of intravesical Resiniferatoxin (RTX) on lower urinary tract symptoms, urodynamic parameters, and quality of life of patients with urodynamic increased bladder sensation. Eur Urol 2006; 50(6): 1299-305.
68. Lazzeri M, Beneforti P, Spinelli M, Zanollo A, Barbagli G, Turini D. Intravesical resiniferatoxin for the treatment of hypersensitive disorder: a randomized placebo controlled study. J Urol 2000; 164(3 Pt 1): 676-9.
69. Chen TY, Corcos J, Camel M, Ponsot Y, Tu le M. Prospective, randomized, double-blind study of safety and tolerability of intravesical resiniferatoxin (RTX) in interstitial cystitis (IC). Int Urogynecol J Pelvic Floor Dysfunct 2005; 16(4): 293-7.
70. Payne CK, Mosbaugh PG, Forrest JB, et al. ICOS RTX Study Group (Resiniferatoxin Treatment for Interstitial Cystitis). Intravesical resiniferatoxin for the treatment of interstitial cystitis: a randomized, double-blind, placebo controlled trial. J Urol 2005; 173(5): 1590-4.
71. Brown DL, Fink BR. The history of neural blockade and pain management. In: Cousins MJ, Bridenbaugh PO, Eds. Neural blockade in clinical anesthesia and management of pain, 3rd ed. Philadelphia: Lippincott-Raven 1998; pp 3-34.
72. Kissin I. Vanilloid-induced conduction analgesia: selective, dosedependent, long-lasting, with a low level of potential neurotoxicity. Anesth Analg 2008; 107(1): 271-81.
73. Acs G, Palkovits M, Blumberg P.M. Comparison of [3H]resiniferatoxin binding by the vanilloid(capsaicin) receptor in dorsal root ganglia, spinal cord, dorsal vagal complex, sciatic and vagal nerve and urinary bladder of the rat. Life Sci 1994; 55: 1017-26.
74. Guo A, Vulchanova L, Wang J, Li X, Elde R. Immunocytochemical localization of the vanilloid receptor 1 (VR1), relationship to neuropeptides, the P2X3 purinoceptor and IB4 binding sites. Eur J Neurosci 1999; 11: 946-58.
75. Caudle RM, Karai L, Mena N, et al. Resiniferatoxin-induced loss of plasma membrane in vanilloid receptor expressing cells. Neurotoxicology 2003; 24(6): 895-908.
76. Gover TD, Kao JP, Weinreich D. Calcium signaling in single peripheral sensory nerve terminals. J Neurosci 2003; 23(12): 4793-7.
77. Tender GC, Walbridge S, Olah Z, et al. Selective ablation of nociceptive neurons for elimination of hyperalgesia and neurogenic inflammation. J Neurosurg 2005; 102(3): 522-5.
78. Neubert JK, Mannes A, Laszlo K, et al. Perineural resiniferatoxin selectively inhibits inflammatory hyperalgesia. Mol Pain 2008; 4: 3.
79. Kissin I, Freitas CF, Bradley EL Jr. Perineural resiniferatoxin prevents the development of hyperalgesia produced by loose ligation of the sciatic nerve in rats. Anesth Analg 2007; 104(5): 1210-6.
80. Brull R, Perlas A, Chan VW. Ultrasound-guided peripheral nerve blockade. Curr Pain Headache Rep 2007; 11(1): 25-32.
81. Peng PW, Tumber PS. Ultrasound-guided interventional procedures for patients with chronic pelvic pain-a description of techniques and review of literature. Pain Physician 2008; 11(2): 215-24.
82. Iadarola MJ, Mannes AJ. The vanilloid agonist resiniferatoxin for interventional-based pain control. Curr Top Med Chem 2011; 11(17): 2171-9.
83. Mannes M, Hughes M, Quezado Z, et al. A potent TRPV1 agonist: Intrathecal administration to treat severe pain associated with advanced cancer-case report. J Pain 2010; 11(4): S43.
84. Evans AT, Gordge PC, Sahni V, Evans FJ. The potent irritancy of the daphnane orthoester, resiniferatoxin, exhibits features of a mixed aetiology. J Pharm Pharmacol 1992; 44(4): 361-3.
85. Tanaka N, Yamaga M, Tateyama S, Uno T, Tsuneyoshi I, Takasaki M. The effect of pulsed radiofrequency current on mechanical allodynia induced with resiniferatoxin in rats. Anesth Analg 2010; 111(3): 784-90.
86. Ossipov MH, Bian D, Malan TP Jr, Lai J, Porreca F. 10. Lack of involvement of capsaicin-sensitive primary afferents in nerveligation injury induced tactile allodynia in rats. Pain 1999; 79(2-3): 127-33.
87. Traub RJ, Allen B, Humphrey E, Ruda MA. Analysis of calcitonin gene-related peptide-like immunoreactivity in the cat dorsal spinal cord and dorsal root ganglia provide evidence for a multisegmental projection of nociceptive C-fiber primary afferents. J Comp Neurol 1990; 302(3): 562-74.
88. Traub RJ, Solodkin A, Ruda MA. Calcitonin gene-related peptide immunoreactivity in the cat lumbosacral spinal cord and the effects of multiple dorsal rhizotomies. J Comp Neurol 1989; 287(2): 225-37.
89. Traub RJ, Iadarola MJ, Ruda MA. Effect of multiple dorsal rhizotomies on calcitonin gene-related peptide-like immunoreactivity in the lumbosacral dorsal spinal cord of the cat: a radioimmunoassay analysis. Peptides 1989; 10(5): 979-83.
90. Crutcher KA, Brothers L, Davis JN. Sympathetic noradrenergic sprouting in response to central cholinergic denervation; a histochemical study of neuronal sprouting in the rat hippocampal formation. Brain Res 1981; 210(1-2): 115-28.
91. Madison R, Davis JN. Sprouting of noradrenergic fibers in hippocampus after medial septal lesions: contributions of the central and peripheral nervous systems. Exp Neurol 1983; 80(1): 167-77.
92. Gracely RH, Lynch SA, Bennett GJ. Painful neuropathy: altered central processing maintained dynamically by peripheral input. Pain 1992; 51(2): 175-94.
93. Roh EJ, Keller JM, Olah Z, Iadarola MJ, Jacobson KA. Structureactivity relationships of 1,4-dihydropyridines that act as enhancers of the vanilloid receptor 1 (TRPV1). Bioorg Med Chem 2008; 16(20): 9349-58.
94. Kaszas K, Keller JM, Coddou C, et al. Small molecule positive allosteric modulation of TRPV1 activation by vanilloids and acidic pH. J Pharmacol Exp Ther 2012; 340(1): 152-60.