HCN1 channels as targets for anesthetic and nonanesthetic propofol analogs in the amelioration of mechanical and thermal hyperalgesia in a mouse model of neuropathic pains

Journal of Pharmacology and Experimental Therapeutics

Volumn 345, Issue 3, 2013, Pages 363-373

  Tibbs, Gareth R ^a,b   Rowley, Thomas J ^b   Sanford, R Lea ^b   Herold, Karl F ^c   Proekt, Alex ^c   Hemmings, Hugh C ^c   Andersen, Olaf S ^a,b   Goldstein, Peter A ^c   Flood, Pamela D ^b  

^a Columbia University ^*  (United States)

^b Neuroscience Center of Excellence   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 DI SEC BUTYLPHENOL; 2,4 DI TERTBUTYLPHENOL; 2,6 DI SEC BUTYLPHENOL; 2,6 DI TERTBUTYLPHENOL; 4 AMINOBUTYRIC ACID A RECEPTOR; ANALGESIC AGENT; ANESTHETIC AGENT; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE REGULATED CHANNEL 1; NERVE PROTEIN; PROPOFOL; UNCLASSIFIED DRUG;

ANALGESIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFECT; DRUG MEGADOSE; DRUG POTENCY; DRUG TARGETING; FEMALE; HYDROPHOBICITY; HYPERALGESIA; LATENT PERIOD; LIPID BILAYER; MOUSE; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL;

EID: 84878099599     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.113.203620     Document Type: Article

References (59)

1. Ahrens J, Haeseler G, Leuwer M, Mohammadi B, Krampfl K, Dengler R, and Bufler J (2004) 2,6 di-tert-butylphenol, a nonanesthetic propofol analog, modulates a1b glycine receptor function in a manner distinct from propofol. Anesth Analg 99: 91-96.
2. Ahrens J, Leuwer M, de la Roche J, Foadi N, Krampfl K, and Haeseler G (2009) The non-anaesthetic propofol analogue 2,6-di-tert-butylphenol fails to modulate GABAA receptor function. Pharmacology 83:95-98.
3. Andersen OS (2008) Perspectives on how to drug an ion channel. J Gen Physiol 131: 395-397.
4. Anker-Møller E, Spangsberg N, Arendt-Nielsen L, Schultz P, Kristensen MS, and Bjerring P (1991) Subhypnotic doses of thiopentone and propofol cause analgesia to experimentally induced acute pain. Br J Anaesth 66:185-188.
5. Briggs LP, Dundee JW, Bahar M, and Clarke RS (1982) Comparison of the effect of diisopropyl phenol (ICI 35, 868) and thiopentone on response to somatic pain. Br J Anaesth 54:307-311.
6. Cacheaux LP, Topf N, Tibbs GR, Schaefer UR, Levi R, Harrison NL, Abbott GW, and Goldstein PA (2005) Impairment of hyperpolarization-activated, cyclic nucleotide-gated channel function by the intravenous general anesthetic propofol. J Pharmacol Exp Ther 315:517-525.
7. Chaplan SR, Guo HQ, Lee DH, Luo L, Liu C, Kuei C, Velumian AA, Butler MP, Brown SM, and Dubin AE (2003) Neuronal hyperpolarization-activated pacemaker channels drive neuropathic pain. J Neurosci 23:1169-1178.
8. Chen X, Shu S, and Bayliss DA (2005) Suppression of ih contributes to propofolinduced inhibition of mouse cortical pyramidal neurons. J Neurophysiol 94: 3872-3883.
9. Cheng SS, Yeh J, and Flood P (2008) Anesthesia matters: Patients anesthetized with propofol have less postoperative pain than those anesthetized with isoflurane. Anesth Analg 106:264-269.
10. Costigan M, Scholz J, and Woolf CJ (2009) Neuropathic pain: A maladaptive response of the nervous system to damage. Annu Rev Neurosci 32:1-32.
11. Dawidowicz AL, Fijalkowska A, Nestorowicz A, Kalitynski R, and Trojanowski T (2003) Cerebrospinal fluid and blood propofol concentration during total intravenous anaesthesia for neurosurgery. Br J Anaesth 90:84-86.
12. Dawidowicz AL and Kalitynski R (2003) HPLC investigation of free and bound propofol in human plasma and cerebrospinal fluid. Biomed Chromatogr 17:447-452.
13. Dawidowicz AL, Kalitynski R, Nestorowicz A, and Fijalkowska A (2002) Changes of propofol concentration in cerebrospinal fluid during continuous infusion. Anesth Analg 95:1282-1284.
14. Dib-Hajj SD, Black JA, and Waxman SG (2009) Voltage-gated sodium channels: Therapeutic targets for pain. Pain Med 10:1260-1269.
15. Dray A (2008) Neuropathic pain: Emerging treatments. Br J Anaesth 101:48-58.
16. Eger EI, 2nd, Tang M, Liao M, Laster MJ, Solt K, Flood P, Jenkins A, Raines D, Hendrickx JF, and Shafer SL, et al. (2008) Inhaled anesthetics do not combine to produce synergistic effects regarding minimum alveolar anesthetic concentration in rats. Anesth Analg 107:479-485.
17. Emery EC, Young GT, Berrocoso EM, Chen L, and McNaughton PA (2011) HCN2 ion channels play a central role in inflammatory and neuropathic pain. Science 333: 1462-1466.
18. Emery EC, Young GT, and McNaughton PA (2012) HCN2 ion channels: An emerging role as the pacemakers of pain. Trends Pharmacol Sci 33:456-463.
19. Engdahl O, Abrahams M, Björnsson A, Vegfors M, Norlander B, Ahlner J, and Eintrei C (1998) Cerebrospinal fluid concentrations of propofol during anaesthesia in humans. Br J Anaesth 81:957-959.
20. Erenmemisoglu A, Madenoglu H, and Tekol Y (1993) Antinociceptive effect of propofol on somatic and visceral pain in subhypnotic doses. Curr Ther Res 53:677-681.
21. Franks NP (2008) General anaesthesia: From molecular targets to neuronal pathways of sleep and arousal. Nat Rev Neurosci 9:370-386.
22. Franks NP and Lieb WR (1985) Mapping of general anaesthetic target sites provides a molecular basis for cutoff effects. Nature 316:349-351.
23. Frölich MA, Price DD, Robinson ME, Shuster JJ, Theriaque DW, and Heft MW (2005) The effect of propofol on thermal pain perception. Anesth Analg 100: 481-486.
24. Haeseler G and Leuwer M (2003) High-affinity block of voltage-operated rat IIA neuronal sodium channels by 2,6 di-tert-butylphenol, a propofol analogue. Eur J Anaesthesiol 20:220-224.
25. Ingólfsson HI and Andersen OS (2010) Screening for small molecules' bilayermodifying potential using a gramicidin-based fluorescence assay. Assay Drug Dev Technol 8:427-436.
26. Ingólfsson HI and Andersen OS (2011) Alcohol's effects on lipid bilayer properties. Biophys J 101:847-855.
27. Ingólfsson HI, Sanford RL, Kapoor R, and Andersen OS (2010) Gramicidin-based fluorescence assay; for determining small molecules potential for modifying lipid bilayer properties. J Vis Exp 44:2131.
28. James R and Glen JB (1980) Synthesis, biological evaluation, and preliminary structure-activity considerations of a series of alkylphenols as intravenous anesthetic agents. J Med Chem 23:1350-1357.
29. Jarvis MF, Honore P, Shieh CC, Chapman M, Joshi S, Zhang XF, Kort M, Carroll W, Marron B, and Atkinson R, et al. (2007) A-803467, a potent and selective Nav1.8 sodium channel blocker, attenuates neuropathic and inflammatory pain in the rat. Proc Natl Acad Sci USA 104:8520-8525.
30. Jensen TS, Madsen CS, and Finnerup NB (2009) Pharmacology and treatment of neuropathic pains. Curr Opin Neurol 22:467-474.
31. Jiang YQ, Xing GG, Wang SL, Tu HY, Chi YN, Li J, Liu FY, Han JS, and Wan Y (2008) Axonal accumulation of hyperpolarization-activated cyclic nucleotide-gated cation channels contributes to mechanical allodynia after peripheral nerve injury in rat. Pain 137:495-506.
32. Kouranova EV, Strassle BW, Ring RH, Bowlby MR, and Vasilyev DV (2008) Hyperpolarization-activated cyclic nucleotide-gated channel mRNA and protein expression in large versus small diameter dorsal root ganglion neurons: Correlation with hyperpolarization-activated current gating. Neuroscience 153:1008-1019.
33. Krasowski MD, Jenkins A, Flood P, Kung AY, Hopfinger AJ, and Harrison NL (2001) General anesthetic potencies of a series of propofol analogs correlate with potency for potentiation of g-aminobutyric acid (GABA) current at the GABAA receptor but not with lipid solubility. J Pharmacol Exp Ther 297:338-351.
34. Lee DH, Chang L, Sorkin LS, and Chaplan SR (2005) Hyperpolarization- activated, cation-nonselective, cyclic nucleotide-modulated channel blockade alleviates mechanical allodynia and suppresses ectopic discharge in spinal nerve ligated rats. J Pain 6:417-424.
35. Lingamaneni R, Krasowski MD, Jenkins A, Truong T, Giunta AL, Blackbeer J, MacIver MB, Harrison NL, and Hemmings HC, Jr (2001) Anesthetic properties of 4-iodopropofol: Implications for mechanisms of anesthesia. Anesthesiology 94: 1050-1057.
36. Lundbaek JA, Collingwood SA, Ingólfsson HI, Kapoor R, and Andersen OS (2010) Lipid bilayer regulation of membrane protein function: Gramicidin channels as molecular force probes. J R Soc Interface 7:373-395.
37. Lyashchenko AK, Redd KJ, Yang J, and Tibbs GR (2007) Propofol inhibits HCN1 pacemaker channels by selective association with the closed states of the membrane embedded channel core. J Physiol 583:37-56.
38. Mayer ML and Westbrook GL (1983) A voltage-clamp analysis of inward (anomalous) rectification in mouse spinal sensory ganglion neurones. J Physiol 340: 19-45.
39. McClure KJ, Maher M, Wu N, Chaplan SR, Eckert WA, 3rd, Lee DH, Wickenden AD, Hermann M, Allison B, and Hawryluk N, et al. (2011) Discovery of a novel series of selective HCN1 blockers. Bioorg Med Chem Lett 21:5197-5201.
40. Momin A, Cadiou H, Mason A, and McNaughton PA (2008) Role of the hyperpolarization-activated current Ih in somatosensory neurons. J Physiol 586: 5911-5929.
41. Nishiyama T, Matsukawa T, and Hanaoka K (2004) Intrathecal propofol has analgesic effects on inflammation-induced pain in rats. Can J Anaesth 51:899-904.
42. Nury H, Van Renterghem C, Weng Y, Tran A, Baaden M, Dufresne V, Changeux JP, Sonner JM, Delarue M, and Corringer PJ (2011) X-ray structures of general anaesthetics bound to a pentameric ligand-gated ion channel. Nature 469:428-431.
43. Orio P, Madrid R, de la Peña E, Parra A, Meseguer V, Bayliss DA, Belmonte C, and Viana F (2009) Characteristics and physiological role of hyperpolarization activated currents in mouse cold thermoreceptors. J Physiol 587:1961-1976.
44. Ouyang W, Wang G, and Hemmings HC, Jr (2003) Isoflurane and propofol inhibit voltage-gated sodium channels in isolated rat neurohypophysial nerve terminals. Mol Pharmacol 64:373-381.
45. Pistis M, Belelli D, Peters JA, and Lambert JJ (1997) The interaction of general anaesthetics with recombinant GABAA and glycine receptors expressed in Xenopus laevis oocytes: A comparative study. Br J Pharmacol 122:1707-1719.
46. Rusinova R, Herold KF, Sanford RL, Greathouse DV, Hemmings HC, Jr, and Andersen OS (2011) Thiazolidinedione insulin sensitizers alter lipid bilayer properties and voltage-dependent sodium channel function: Implications for drug discovery. J Gen Physiol 138:249-270.
47. Seltzer Z, Dubner R, and Shir Y (1990) A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 43:205-218.
48. Servin F, Desmonts JM, Haberer JP, Cockshott ID, Plummer GF, and Farinotti R (1988) Pharmacokinetics and protein binding of propofol in patients with cirrhosis. Anesthesiology 69:887-891.
49. Sherman SE and Loomis CW (1994) Morphine insensitive allodynia is produced by intrathecal strychnine in the lightly anesthetized rat. Pain 56:17-29.
50. Smith C, McEwan AI, Jhaveri R, Wilkinson M, Goodman D, Smith LR, Canada AT, and Glass PS (1994) The interaction of fentanyl on the Cp50 of propofol for loss of consciousness and skin incision. Anesthesiology 81:820-828, discussion 26A.
51. Song Y, Connor DT, Doubleday R, Sorenson RJ, Sercel AD, Unangst PC, Roth BD, Gilbertsen RB, Chan K, and Schrier DJ, et al. (1999) Synthesis, structure-activity relationships, and in vivo evaluations of substituted di-tert-butylphenols as a novel class of potent, selective, and orally active cyclooxygenase-2 inhibitors. 1. Thiazolone and oxazolone series. J Med Chem 42:1151-1160.
52. Sun YY, Li KC, and Chen J (2005) Evidence for peripherally antinociceptive action of propofol in rats: Behavioral and spinal neuronal responses to subcutaneous bee venom. Brain Res 1043:231-235.
53. Tan T, Bhinder R, Carey M, and Briggs L (2010) Day-surgery patients anesthetized with propofol have less postoperative pain than those anesthetized with sevoflurane. Anesth Analg 111:83-85.
54. Tu H, Deng L, Sun Q, Yao L, Han JS, and Wan Y (2004) Hyperpolarization- activated, cyclic nucleotide-gated cation channels: Roles in the differential electrophysiological properties of rat primary afferent neurons. J Neurosci Res 76:713-722.
55. Udesky JO, Spence NZ, Achiel R, Lee C, and Flood P (2005) The role of nicotinic inhibition in ketamine-induced behavior. Anesth Analg 101:407-411.
56. Vo T, Rice AS, and Dworkin RH (2009) Non-steroidal anti-inflammatory drugs for neuropathic pain: How do we explain continued widespread use? Pain 143:169-171.
57. Yao H, Donnelly DF, Ma C, and LaMotte RH (2003) Upregulation of the hyperpolarization-activated cation current after chronic compression of the dorsal root ganglion. J Neurosci 23:2069-2074.
58. Yeon KY, Chung G, Kim YH, Hwang JH, Davies AJ, Park MK, Ahn DK, Kim JS, Jung SJ, and Oh SB (2011) Eugenol reverses mechanical allodynia after peripheral nerve injury by inhibiting hyperpolarization-activated cyclic nucleotide-gated (HCN) channels. Pain 152:2108-2116.
59. Ying SW, Abbas SY, Harrison NL, and Goldstein PA (2006) Propofol block of I(h) contributes to the suppression of neuronal excitability and rhythmic burst firing in thalamocortical neurons. Eur J Neurosci 23:465-480.