Targeting of sodium channel blockers into nociceptors to produce long-duration analgesia: A systematic study and review

British Journal of Pharmacology

Volumn 164, Issue 1, 2011, Pages 48-58

  Roberson, D P ^a,b,c   Binshtok, A M ^a,d   Blasl, F ^a   Bean, B P ^b   Woolf, C J ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^d HEBREW UNIVERSITY   (Israel)

Author keywords

differential block; lidocaine; long duration analgesia; nerve block; QX 314; regional anaesthesia; sodium channel blockers; targeted delivery; TRPV1 channels

Indexed keywords

LIDOCAINE; LIDOCAINE ETHOBROMIDE; SODIUM CHANNEL BLOCKING AGENT; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1 AGONIST; VANILLOID RECEPTOR AGONIST;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; AREA UNDER THE CURVE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG MEGADOSE; DRUG POTENTIATION; DRUG TARGETING; GRIP STRENGTH; MALE; MOTOR DYSFUNCTION; NERVE BLOCK; NERVE COMPRESSION; NERVE POTENTIAL; NERVE STIMULATION; NOCICEPTIVE RECEPTOR; NONHUMAN; PAIN; PRIORITY JOURNAL; RAT; REVIEW; SCIATIC NERVE; SYSTEMATIC REVIEW (TOPIC); THERMAL STIMULATION;

ANALGESICS; ANIMALS; DRUG DELIVERY SYSTEMS; LIDOCAINE; MALE; NOCICEPTORS; PAIN; RATS; SENSORY RECEPTOR CELLS; SODIUM CHANNEL BLOCKERS; TRPV CATION CHANNELS;

EID: 79960180415     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2011.01391.x     Document Type: Review

References (69)

1. Ahern CA, Eastwood AL, Dougherty DA, Horn R, (2008). Electrostatic contributions of aromatic residues in the local anesthetic receptor of voltage-gated sodium channels. Circ Res 102: 86-94.
2. Berberich G, Reader A, Drum M, Nusstein J, Beck M, (2009). A prospective, randomized, double-blind comparison of the anesthetic efficacy of two percent lidocaine with 1:100,000 and 1:50,000 epinephrine and three percent mepivacaine in the intraoral, infraorbital nerve block. J Endod 35: 1498-1504.
3. Binshtok AM, Bean BP, Woolf CJ, (2007). Inhibition of nociceptors by TRPV1-mediated entry of impermeant sodium channel blockers. Nature 449: 607-610. (Pubitemid 47525153)
4. Binshtok AM, Gerner P, Oh SB, Puopolo M, Suzuki S, Roberson DP, et al,. (2009a). Coapplication of lidocaine and the permanently charged sodium channel blocker QX-314 produces a long-lasting nociceptive blockade in rodents. Anesthesiology 111: 127-137.
5. Binshtok AM, et al,. (2009b). Activation of TRPA1 As Well As TRPV1 Channels by Lidocaine Allows Entry of QX-314 into Nociceptors to Produce A Pain Selective Sodium Channel Block. Society for Neuroscience Meeting: Chikago, IL.
6. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D, (1997). The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824. (Pubitemid 27462969)
7. Chen J, Kim D, Bianchi BR, Cavanaugh EJ, Faltynek CR, Kym PR, et al,. (2009). Pore dilation occurs in TRPA1 but not in TRPM8 channels. Mol Pain 5: 3.
8. Chevrier P, Vijayaragavan K, Chahine M, (2004). Differential modulation of Nav1.7 and Nav1.8 peripheral nerve sodium channels by the local anesthetic lidocaine. Br J Pharmacol 142: 576-584. (Pubitemid 38869872)
9. Chung MK, Guler AD, Caterina MJ, (2008). TRPV1 shows dynamic ionic selectivity during agonist stimulation. Nat Neurosci 11: 555-564. (Pubitemid 351595196)
10. Clapham DE, Runnels LW, Strübing C, (2001). The TRP ion channel family. Nat Rev Neurosci 2: 387-396. (Pubitemid 33674795)
11. Cornett PM, Matta JA, Ahern GP, (2008). General anesthetics sensitize the capsaicin receptor transient receptor potential V1. Mol Pharmacol 74: 1261-1268.
12. Davies RJ, (2003). Buffering the pain of local anaesthetics: a systematic review. Emerg Med (Fremantle) 15: 81-88. (Pubitemid 36331342)
13. Dib-Hajj SD, Binshtok AM, Cummins TR, Jarvis MF, Samad T, Zimmermann K, (2009). Voltage-gated sodium channels in pain states: role in pathophysiology and targets for treatment. Brain Res Rev 60: 65-83.
14. Dillane D, Finucane BT, (2010). Local anesthetic systemic toxicity. Can J Anaesth 57: 368-380.
15. Dillane D, Tsui BC, (2010). From basic concepts to emerging technologies in regional anesthesia. Curr Opin Anaesthesiol 23: 663-669.
16. Enneking F, Wedel D, Horlocker T, (2009). The Lower Extremity: Somatic Blockade, 4th edn. Lippincott Williams & Wilkins: Philadelphia, PA.
17. Frazier DT, Narahashi T, Yamada M, (1970). The site of action and active form of local anesthetics. II. Experiments with quaternary compounds. J Pharmacol Exp Ther 171: 45-51.
18. Fredrickson MJ, Krishnan S, Chen CY, (2010). Postoperative analgesia for shoulder surgery: a critical appraisal and review of current techniques. Anaesthesia 65: 608-624.
19. Gustafsson H, Akesson J, Lau CL, Williams D, Miller L, Yap S, et al,. (2009). A comparison of two formulations of intradermal capsaicin as models of neuropathic pain in healthy volunteers. Br J Clin Pharmacol 68: 511-517.
20. Hargreaves K, Dubner R, Brown F, Flores C, Joris J, (1988). A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32: 77-88.
21. Harrison N, Nau C, (2008). Sensitization of nociceptive ion channels by inhaled anesthetics-a pain in the gas? Mol Pharmacol 74: 1180-1182.
22. Hawkins JL, (2010). Epidural analgesia for labor and delivery. N Engl J Med 362: 1503-1510.
23. Hellwig N, Plant TD, Janson W, Schafer M, Schultz G, Schaefer M, (2004). TRPV1 acts as proton channel to induce acidification in nociceptive neurons. J Biol Chem 279: 34553-34561. (Pubitemid 39318084)
24. Hille B, (1977a). Local anesthetics: hydrophilic and hydrophobic pathways for the drug-receptor reaction. J Gen Physiol 69: 497-515. (Pubitemid 8086978)
25. Hille B, (1977b). The pH-dependent rate of action of local anesthetics on the node of Ranvier. J Gen Physiol 69: 475-496. (Pubitemid 8086977)
26. Hoffmann T, Sauer SK, Horch RE, Reeh PW, (2008). Sensory transduction in peripheral nerve axons elicits ectopic action potentials. J Neurosci 28: 6281-6284.
27. Hogan MV, Grant RE, Lee L Jr, (2009). Analgesia for total hip and knee arthroplasty: a review of lumbar plexus, femoral, and sciatic nerve blocks. Am J Orthop (Belle Mead NJ) 38: E129-E133.
28. Kim HY, Kim K, Li HY, Chung G, Park CK, Kim JS, et al,. (2010). Selectively targeting pain in the trigeminal system. Pain 150: 29-40.
29. Leffler A, Herzog RI, Dib-Hajj SD, Waxman SG, Cummins TR, (2005). Pharmacological properties of neuronal TTX-resistant sodium channels and the role of a critical serine pore residue. Pflugers Arch 451: 454-463. (Pubitemid 41719577)
30. Leffler A, Fischer MJ, Rehner D, Kienel S, Kistner K, Sauer SK, et al,. (2008). The vanilloid receptor TRPV1 is activated and sensitized by local anesthetics in rodent sensory neurons. J Clin Invest 118: 763-776. (Pubitemid 351206564)
31. Lemke KA, Dawson SD, (2000). Local and regional anesthesia. Vet Clin North Am Small Anim Pract 30: 839-857. (Pubitemid 30483045)
32. Lim TK, Macleod BA, Ries CR, Schwarz SK, (2007). The quaternary lidocaine derivative, QX-314, produces long-lasting local anesthesia in animal models in vivo. Anesthesiology 107: 305-311. (Pubitemid 47196495)
33. Lirk P, Haller I, Colvin HP, Frauscher S, Kirchmair L, Gerner P, et al,. (2007). In vitro, lidocaine-induced axonal injury is prevented by peripheral inhibition of the p38 mitogen-activated protein kinase, but not by inhibiting caspase activity. Anesth Analg 105: 1657-1664. Table of contents. (Pubitemid 350190560)
34. Liu H, Atkins J, Kass RS, (2003). Common molecular determinants of flecainide and lidocaine block of heart Na+ channels: evidence from experiments with neutral and quaternary flecainide analogues. J Gen Physiol 121: 199-214. (Pubitemid 36292990)
35. Luis-Delgado OE, Barrot M, Rodeau JL, Schott G, Benbouzid M, Poisbeau P, et al,. (2006). Calibrated forceps: a sensitive and reliable tool for pain and analgesia studies. J Pain 7: 32-39. (Pubitemid 43102463)
36. Matta JA, Cornett PM, Miyares RL, Abe K, Sahibzada N, Ahern GP, (2008). General anesthetics activate a nociceptive ion channel to enhance pain and inflammation. Proc Natl Acad Sci U S A 105: 8784-8789. (Pubitemid 351987757)
37. McNulty MM, Edgerton GB, Shah RD, Hanck DA, Fozzard HA, Lipkind GM, (2007). Charge at the lidocaine binding site residue Phe-1759 affects permeation in human cardiac voltage-gated sodium channels. J Physiol 581 (Pt 2): 741-755. (Pubitemid 46831768)
38. Meyers JR, MacDonald RB, Duggan A, Lenzi D, Standaert DG, Corwin JT, et al,. (2003). Lighting up the senses: FM1-43 loading of sensory cells through nonselective ion channels. J Neurosci 23: 4054-4065. (Pubitemid 36958424)
39. Momin A, Wood JN, (2008). Sensory neuron voltage-gated sodium channels as analgesic drug targets. Curr Opin Neurobiol 18: 383-388.
40. Muroi Y, Chanda B, (2009). Local anesthetics disrupt energetic coupling between the voltage-sensing segments of a sodium channel. J Gen Physiol 133: 1-15.
41. Murray JM, Derbyshire S, Shields MO, (2010). Lower limb blocks. Anaesthesia 65 (Suppl. 1): 57-66.
42. Nakamura T, Popitz-Bergez F, Birknes J, Strichartz GR, (2003). The critical role of concentration for lidocaine block of peripheral nerve in vivo: studies of function and drug uptake in the rat. Anesthesiology 99: 1189-1197. (Pubitemid 37339467)
43. Neal JM, Bernards CM, Butterworth JFT, Di Gregorio G, Drasner K, Hejtmanek MR, et al,. (2010). ASRA practice advisory on local anesthetic systemic toxicity. Reg Anesth Pain Med 35: 152-161.
44. O'Donnell B, Riordan J, Ahmad I, Iohom G, (2010). A clinical evaluation of block characteristics using one milliliter 2% lidocaine in ultrasound-guided axillary brachial plexus block. Anesth Analg 111: 808-810.
45. Oseguera AJ, Islas LD, Garcia-Villegas R, Rosenbaum T, (2007). On the mechanism of TBA block of the TRPV1 channel. Biophys J 92: 3901-3914. (Pubitemid 46910577)
46. Perez-Castro R, Patel S, Garavito-Aguilar ZV, Rosenberg A, Recio-Pinto E, Zhang J, et al,. (2009). Cytotoxicity of local anesthetics in human neuronal cells. Anesth Analg 108: 997-1007.
47. Power I, McCormack JG, Myles PS, (2010). Regional anaesthesia and pain management. Anaesthesia 65 (Suppl. 1): 38-47.
48. Premkumar LS, Ahern GP, (2000). Induction of vanilloid receptor channel activity by protein kinase C. Nature 408: 985-990. (Pubitemid 32101646)
49. Premkumar LS, Agarwal S, Steffen D, (2002). Single-channel properties of native and cloned rat vanilloid receptors. J Physiol 545 (Pt 1): 107-117. (Pubitemid 35386130)
50. Priest BT, (2009). Future potential and status of selective sodium channel blockers for the treatment of pain. Curr Opin Drug Discov Devel 12: 682-692.
51. Ragsdale DS, McPhee JC, Scheuer T, Catterall WA, (1994). Molecular determinants of state-dependent block of Na+ channels by local anesthetics. Science 265: 1724-1728. (Pubitemid 24314907)
52. Ragsdale DS, McPhee JC, Scheuer T, Catterall WA, (1996). Common molecular determinants of local anesthetic, antiarrhythmic, and anticonvulsant block of voltage-gated Na+ channels. Proc Natl Acad Sci U S A 93: 9270-9275. (Pubitemid 26282053)
53. Raisinghani M, Pabbidi RM, Premkumar LS, (2005). Activation of transient receptor potential vanilloid 1 (TRPV1) by resiniferatoxin. J Physiol 567 (Pt 3): 771-786. (Pubitemid 41387825)
54. Ries CR, Pillai R, Chung CC, Wang JT, MacLeod BA, Schwarz SK, (2009). QX-314 produces long-lasting local anesthesia modulated by transient receptor potential vanilloid receptors in mice. Anesthesiology 111: 122-126.
55. Satoh J, Yamakage M, (2009). Desflurane induces airway contraction mainly by activating transient receptor potential A1 of sensory C-fibers. J Anesth 23: 620-623.
56. Schwarz W, Palade PT, Hille B, (1977). Local anesthetics. Effect of pH on use-dependent block of sodium channels in frog muscle. Biophys J 20: 343-368. (Pubitemid 8242214)
57. Schwarz SK, Cheung HM, Ries CR, Lee SM, Wang JT, MacLeod BA, (2010). Lumbar intrathecal administration of the quaternary lidocaine derivative, QX-314, produces irritation and death in mice. Anesthesiology 113: 438-444.
58. Scott NB, (2010). Wound infiltration for surgery. Anaesthesia 65 (Suppl. 1): 67-75.
59. Sheets MF, Hanck DA, (2007). Outward stabilization of the S4 segments in domains III and IV enhances lidocaine block of sodium channels. J Physiol 582 (Pt 1): 317-334. (Pubitemid 46993577)
60. Simon D, Seznec H, Gansmuller A, Carelle N, Weber P, Metzger D, et al,. (2004). Friedreich ataxia mouse models with progressive cerebellar and sensory ataxia reveal autophagic neurodegeneration in dorsal root ganglia. J Neurosci 24: 1987-1995. (Pubitemid 38292812)
61. Strichartz GR, (1973). The inhibition of sodium currents in myelinated nerve by quaternary derivatives of lidocaine. J Gen Physiol 62: 37-57.
62. Takeda D, Nakatsuka T, Papke R, Gu JG, (2003). Modulation of inhibitory synaptic activity by a non-alpha4beta2, non-alpha7 subtype of nicotinic receptors in the substantia gelatinosa of adult rat spinal cord. Pain 101: 13-23. (Pubitemid 36044650)
63. Takeda D, Nakatsuka T, Gu JG, Yoshida M, (2007). The activation of nicotinic acetylcholine receptors enhances the inhibitory synaptic transmission in the deep dorsal horn neurons of the adult rat spinal cord. Mol Pain 3: 26.
64. Vossinakis IC, Stavroulaki P, Paleochorlidis I, Badras LS, (2004). Reducing the pain associated with local anaesthetic infiltration for open carpal tunnel decompression. J Hand Surg Br 29: 399-401. (Pubitemid 38878106)
65. Werdehausen R, Fazeli S, Braun S, Hermanns H, Essmann F, Hollmann MW, et al,. (2009). Apoptosis induction by different local anaesthetics in a neuroblastoma cell line. Br J Anaesth 103: 711-718.
66. Wood JN, Boorman JP, Okuse K, Baker MD, (2004). Voltage-gated sodium channels and pain pathways. J Neurobiol 61: 55-71. (Pubitemid 39287770)
67. Yang BH, Piao ZG, Kim YB, Lee CH, Lee JK, Park K, et al,. (2003). Activation of vanilloid receptor 1 (VR1) by eugenol. J Dent Res 82: 781-785. (Pubitemid 41766107)
68. Yarov-Yarovoy V, McPhee JC, Idsvoog D, Pate C, Scheuer T, Catterall WA, (2002). Role of amino acid residues in transmembrane segments IS6 and IIS6 of the Na+ channel alpha subunit in voltage-dependent gating and drug block. J Biol Chem 277: 35393-35401.
69. Zhang XF, Shieh CC, Chapman ML, Matulenko MA, Hakeem AH, Atkinson RN, et al,. (2010). A-887826 is a structurally novel, potent and voltage-dependent Na(v)1.8 sodium channel blocker that attenuates neuropathic tactile allodynia in rats. Neuropharmacology 59: 201-207.