Endothelin-1 raises excitability and reduces potassium currents in sensory neurons

Brain Research Bulletin

Volumn 79, Issue 6, 2009, Pages 345-350

  Feng, Bihua ^a   Strichartz, Gary ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Endothelin 1; Excitability; Nociceptor; Pain; Potassium channel

Indexed keywords

ENDOTHELIN 1; ISOLECTIN B4;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; ELECTROPHYSIOLOGY; EXCITABILITY; MALE; MEMBRANE STEADY POTENTIAL; NOCICEPTION; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; SPINAL GANGLION; STEADY STATE; VOLTAGE CLAMP;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; CELL SIZE; CELLS, CULTURED; DELAYED RECTIFIER POTASSIUM CHANNELS; ENDOTHELIN-1; GANGLIA, SPINAL; GLYCOPROTEINS; LECTINS; MALE; MEMBRANE POTENTIALS; PATCH-CLAMP TECHNIQUES; POTASSIUM; RATS; RATS, SPRAGUE-DAWLEY; SENSORY RECEPTOR CELLS; TIME FACTORS;

EID: 67449164333     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2009.04.012     Document Type: Article

References (43)

1. Armstrong C.M., and Bezanilla F. Inactivation of the sodium channel II. Gating current experiments. J. Gen. Physiol. 70 (1977) 567-590
2. Beekwilder J.P., O'Leary M.E., van den Broek L.P., van Kempen G.Th.H., Ypey D.L., and van den Berg R.J. Kv1.1 channels of dorsal root ganglion neurons are inhibited by n-butyl-p-aminobenzoate, a promising anesthetic for the treatment of chronic pain. J. Pharmacol. Exp. Ther. 304 (2003) 531-538
3. Bonnington J.K., and McNaughton P.A. Signalling pathways involved in the sensitization of mouse nociceptive neurones by nerve growth factor. J. Physiol. 551 (2003) 433-446
4. + currents generates distinct firing patterns in different subtypes of adult mouse trigeminal ganglion neurones. J. Physiol. 586 (2008) 5101-5118
5. Chi X.X., and Nicol G.D. Manipulation of the potassium channel Kv1.1 and its effect on neuronal excitability on rat sensory neurons. J. Neurophysiol. 98 (2007) 2683-2692
6. Davar G., Hans G., Fareed M.U., Sinnott C., and Strichartz G. Behavioral signs of acute pain produced by application of endothelin-1 to rat sciatic nerve. NeuroReport 9 (1998) 2279-2283
7. Davenport A.P., and Kuc R.E. Cellular expression of isoforms of endothelin-converting enzyme-1 (ECE-1c ECE-1b and ECE-1a) and endothelin-converting enzyme-2. J. Cardiovasc. Pharmacol. 36 (2000) S12-S14
8. de-Melo J.D., Tonussi C.R., D'Orleans-Juste P., and Rae G.A. Effects of endothelin-1 on inflammatory incapacitation of the rat knee joint. J. Cardiovasc. Pharmacol. 31 (1998) S518-S520
9. Dirajlal S., Pauers L.E., and Stucky C.L. Differential response properties of IB(4)-positive and -negative unmyelinated sensory neurons to protons and capsaicin. J. Neurophysiol. 89 (2003) 513-524
10. Dost R., Rostock A., and Rundfeldt C. The anti-hyperalgesic activity of retigabine is mediated by KCNQ potassium channel activation. Naunyn Schmiedeberg's Arch. Pharmacol. 369 (2004) 382-390
11. 2-induced inhibition of potassium currents in rat sensory neurones. J. Physiol. 516 (1999) 163-178
12. Ferreira S.H., Romitelli M., and de Nucci G. Endothelin-1 participation in overt and inflammatory pain. J. Cardiovasc. Pharmacol. 13 (1989) S220-S222
13. Glazebrook P.A., Ramirez A.N., Schild J.H., Shieh C.C., Doan T., Wible B.A., and Kunze D.L. Potassium channels Kv1.1, Kv1. 2 and Kv1. 6 influence excitability of rat visceral sensory neurons. J. Physiol. 541 (2002) 467-482
14. Gokin A.P., Fareed M.U., Pan H.L., Hans G., Strichartz G.R., and Davar G. Local injection of endothelin-1 produces pain-like behavior and excitation of nociceptors in rats. J. Neurosci. 21 (2001) 5358-5366
15. Gold M.S., Levine J.D., and Correa A.M. Modulation of TTX-R INa by PKC and PKA and their role in PGE2-induced sensitization of rat sensory neurons in vitro. J. Neurosci. 18 (1998) 10345-10355
16. Gold M.S., Shuster M.J., and Levine J.D. Characterization of six voltage-gated K+ currents in adult rat sensory neurons. J. Neurophysiol. 75 (1996) 2629-2646
17. Gruss M., Ettorre G., Stehr A.J., Henrich M., Hempelmann G., and Scholtz A. Moderate hypoxia influences excitability and blocks dendrotoxin sensitive K+ currents in rat primary sensory neurones. Mol. Pain 2 (2006) 12
18. Hamill O.P., Marty A., Neher E., Sakmann B., and Sigworth F.J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 39 (1981) 85-100
19. Hodgkin A.L., and Huxley A.F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117 (1952) 500-544
20. Jiang X., Zhang Y.H., Clark J.D., Tempel B.L., and Nicol G.D. Prostaglandin E2 inhibits the potassium current in sensory neurons from hyperalgesic Kv1.1 knockout mice. Neuroscience 119 (2003) 65-72
21. Khodorova A., Montmayeur J.-P., and Strichartz G. Endothelin receptors and pain. J. Pain 10 (2009) 4-28
22. Khodorova A., Navarro B., Jouaville L.S., Murphy J.E., Rice F.L., Mazurkiewicz J.E., Long-Woodward D., Stoffel M., Strichartz G.R., Yukhananov R., and Davar G. Endothelin-B receptor activation triggers an endogenous analgesic cascade at sites of peripheral injury. Nat. Med. 9 (2003) 1055-1061
23. Liu B.-G., Dobretsov M., Stimers J.R., and Zhang J.-M. Tumor necrosis factor-α suppresses sustained potassium currents in rat small diameter sensory neurons. Open Pain J. 1 (2008) 1-7
24. Liu M., Willmott N.J., Michael G.J., and Priestley J.V. Differential pH and capsaicin responses of Griffonia simplicifolia IB4 (IB4)-positive and IB4-negative small sensory neurons. Neuroscience 127 (2004) 659-672
25. Passmore G.M., Selyanko A.A., Mistry M., Al-Qatari M., Marsh S.J., Matthews E.A., Dickenson A.H., Brown T.A., Burbidge S.A., Main M., and Brown D.A. KCNQ/M currents in sensory neurons: significance for pain therapy. J. Neurosci. 23 (2003) 7227-7236
26. Patwardhan A.M., Vela J., Farugia J., Vela K., and Hargreaves K.M. Trigeminal nociceptors express prostaglandin receptors. J. Dent. Res. 87 (2008) 262-266
27. Petruska J.C., Napaporn J., Johnson R.D., Gu J.G., and Cooper B.Y. Subclassified acutely dissociated cells of rat DRG: histochemistry and patterns of capsaicin-, proton-, and ATP-activated currents. J. Neurophysiol. 84 (2000) 2365-2379
28. Plant T.D., Zöllner C., Kepura F., Mousa S.S., Eichhorst J., Schaefer M., Furkert J., Stein C., and Oksche A. Endothelin potentiates TRPV1 via ETA receptor-mediated activation of protein kinase C. Mol. Pain 3 (2007) 35
29. Pomonis J.D., Rogers S.D., Peters C.M., Ghilardi J.R., and Mantyh P.W. Expression and localization of endothelin receptors: implications for the involvement of peripheral glia in nociception. J. Neurosci. 21 (2001) 999-1006
30. Rasband M.N., Park E.W., Vanderah T.W., Lai J., Porreca F., and Trimmer J.S. Distinct potassium channels on pain-sensing neurons. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 13373-13378
31. + channels and their functions in small dorsal root ganglion neurones of rat. J. Physiol. 493 (1996) 393-408
32. B-selective agonists. J. Biol. Chem. 268 (1993) 8547-8553
33. Sculptoreanu A., Aura Kullmann F., and de Groat W.C. Neurokinin 2 receptor-mediated activation of protein kinase C modulates capsaicin responses in DRG neurons from adult rats. Eur. J. Neurosci. 27 (2008) 3171-3181
34. Shu X., and Mendell L.M. Nerve growth factor acutely sensitizes the response of adult rat sensory neurons to capsaicin. Neurosci. Lett. 274 (1999) 159-162
35. 4-positive and -negative nociceptors are functionally distinct. J. Neurosci. 19 (1999) 6497-6505
36. Viana F., and Belmonte C. Potassium channels shape and brake primary sensory neurone excitability. J. Physiol. 586 (2008) 5039-5040
37. + currents influence firing properties of isolectin B4-positive but not isolectin B4-negative primary sensory neurons. J. Neurophysiol. 93 (2005) 3401-3409
38. Wang J.-G., Strong J.A., Xie W., and Zhang J.-M. Local inflammation in rat dorsal root ganglion alters excitability and ion currents in small-diameter sensory neurons. Anesthesiology 107 (2007) 322-332
39. 2+ response via activation of endothelin a receptor in a protein kinase C epsilon-dependent manner in dorsal root ganglion neurons. Neuroscience 137 (2006) 949-960
40. Yang E.K., Takimoto K., Hayashi Y., de Groat W.C., and Yoshimura N. Altered expression of potassium channel subunit mRNA and alpha-dendrotoxin of potassium currents in rat dorsal root ganglion neurons after axotomy. Neuroscience 123 (2004) 867-874
41. + current in rat sensory neurons. J. Physiol. 544 (2002) 385-402
42. A receptors to increase intracellular calcium in model sensory neurons. NeuroReport 12 (2001) 3853-3857
43. Zhou Z., Davar G., and Strichartz G. Endothelin-1 (ET-1) selectively enhances the activation gating of slowly inactivating tetrodotoxin-resistant sodium currents in rat sensory neurons: a mechanism for the pain-inducing actions of ET-1. J. Neurosci. 22 (2002) 6325-6330