Excitability parameters and sensitivity to anemone toxin ATX-II in rat small diameter primary sensory neurones discriminated by Griffonia simplicifolia isolectin IB4

Journal of Physiology

Volumn 588, Issue 1, 2010, Pages 125-137

  Snape, Alistair ^a   Pittaway, James F ^a   Baker, Mark D ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ISOLECTIN B4; SEA ANEMONE TOXIN; SODIUM CHANNEL; SODIUM CHANNEL NAV1.8; TETRODOTOXIN;

ANIMAL TISSUE; ARTICLE; CHANNEL GATING; CHEMOSENSITIVITY; CONTROLLED STUDY; DEPOLARIZATION; GRIFFONIA; GRIFFONIA SIMPLICIFOLIA; NERVE CONDUCTION; NERVE EXCITABILITY; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; SODIUM CURRENT; SPINAL GANGLION;

ACTION POTENTIALS; ANIMALS; CELL SIZE; CELLS, CULTURED; CNIDARIAN VENOMS; DOSE-RESPONSE RELATIONSHIP, DRUG; GANGLIA, SPINAL; NEUROTOXINS; PLANT LECTINS; RATS; RATS, WISTAR; SENSORY RECEPTOR CELLS;

EID: 73549113556     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2009.181107     Document Type: Article

References (51)

1. Abrahamsen B, Zhao J, Asante CO, Cendan CM, Marsh S, Martinez-Barbera JP, Nassar MA, Dickenson AH, Wood JN. The cell and molecular basis of mechanical, cold, and inflammatory pain. Science 2008, 321:702-705.
2. Akopian AN, Sivilotti L, Wood JN. A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 1996, 379:257-262.
3. Akopian AN, Souslova V, England S, Okuse K, Ogata N, Ure J, Smith A, Kerr BJ, McMahon SB, Boyce S, Hill R, Stanfa LC, Dickenson AH, Wood JN. The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat Neurosci 1999, 2:541-548.
4. Averill S, McMahon SB, Clary DO, Reichardt LF, Priestley JV. Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur J Neurosci 1995, 7:1484-1494.
5. Baker M, Bostock H. Depolarization changes the mechanism of accommodation in rat and human motor axons. J Physiol 1989, 411:545-561.
6. Baker MD, Bostock H. Low-threshold, persistent sodium current in rat large dorsal root ganglion neurons in culture. J Neurophysiol 1997, 77:1503-1513.
7. Baker MD, Wood JN. Involvement of Na+ channels in pain pathways. Trends Pharmacol Sci 2001, 22:27-31.
8. Bennett DL, Dmietrieva N, Priestley JV, Clary D, McMahon SB. trkA, CGRP and IB4 expression in retrogradely labelled cutaneous and visceral primary sensory neurones in the rat. Neurosci Lett 1996, 206:33-36.
9. Bennett DL, Michael GJ, Ramachandran N, Munson JB, Averill S, Yan Q, McMahon SB, Priestley JV. A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury. J Neurosci 1998, 18:3059-3072.
10. Black JA, Dib-Hajj S, McNabola K, Jeste S, Rizzo MA, Kocsis JD, Waxman SG. Spinal sensory neurons express multiple sodium channel alpha-subunit mRNAs. Brain Res Mol Brain Res 1996, 43:117-131.
11. Blair NT, Bean BP. Roles of tetrodotoxin (TTX)-sensitive Na+ current, TTX-resistant Na+ current and Ca2+ current in the action potentials of nociceptive sensory neurons. J Neurosci 2002, 22:10277-10290.
12. Blair NT, Bean BP. Role of tetrodotoxin-resistant Na+ current slow inactivation in adaptation of action potential firing in small-diameter dorsal root ganglion neurons. J Neurosci 2003, 23:10338-10350.
13. Bostock H, Grafe P. Activity-dependent excitability changes in normal and demyelinated rat spinal root axons. J Physiol 1985, 365:239-257.
14. Carr RW, Pianova S, Brock JA. The effects of polarizing current on nerve terminal impulses recorded from polymodal and cold receptors in the guinea-pig cornea. J Gen Physiol 2002, 120:395-405.
15. Carr RW, Pianova S, McKemy DD, Brock JA. Action potential initiation in the peripheral terminals of cold-sensitive neurones innervating the guinea-pig cornea. J Physiol 2009, 587:1249-1264.
16. Catterall WA, Cestèle S, Yarov-Yarovoy V, Yu FH, Konoki K, Scheuer T. Voltage-gated ion channels and gating modifier toxins. Toxicon 2007, 49:124-141.
17. Choi JS, Dib-Hajj SD, Waxman SG. Differential slow inactivation and use-dependent inhibition of NaV1.8 channels contribute to distinct firing properties in IB4+ and IB4- DRG neurons. J Neurophysiol 2007, 97:1258-1265.
18. Cox JJ, Reimann F, Nicholas AK, Thornton G, Roberts E, Springell K, Karbani G, Jafri H, Mannan J, Raashid Y, Al-Gazali L, Hamamy H, Valente EM, Gorman S, Williams R, McHale DP, Wood JN, Gribble FM, Woods CG. An SCN9A channelopathy causes congenital inability to experience pain. Nature 2006, 444:894-898.
19. Cummins TR, Dib-Hajj SD, Black JA, Akopian AN, Wood JN, Waxman SG. A novel persistent tetrodotoxin-resistant sodium current in SNS-null and wild-type small primary sensory neurons. J Neurosci 1999, 19:RC43.
20. Cummins TR, Dib-Hajj SD, Waxman SG. Electrophysiological properties of mutant NaV1.7 sodium channels in a painful inherited neuropathy. J Neurosci 2004, 24:8232-8236.
21. De Col R, Messlinger K, Carr RW. Conduction velocity is regulated by sodium channel inactivation in unmyelinated axons innervating the rat cranial meninges. J Physiol 2008, 586:1089-1103.
22. Fang X, Djouhri L, McMullan S, Berry C, Waxman SG, Okuse K, Lawson SN. Intense isolectin-B4 binding in rat dorsal root ganglion neurons distinguishes C-fibre nociceptors with broad action potentials and high NaV1.9 expression. J Neurosci 2006, 26:7281-7292.
23. Fertleman CR, Baker MD, Parker KA, Moffatt S, Elmslie FV, Abrahamsen B, Ostman J, Klugbauer N, Wood JN, Gardiner RM, Rees M. SCN9A mutations in paroxysmal extreme pain disorder: allelic variants underlie distinct channel defects and phenotypes. Neuron 2006, 52:767-774.
24. Foulkes T, Nassar MA, Lane T, Matthews EA, Baker MD, Gerke V, Okuse K, Dickenson AH, Wood JN. Deletion of annexin 2 light chain p11 in nociceptors causes deficits in somatosensory coding and pain behaviour. J Neurosci 2006, 26:10499-10507.
25. Fullmer JM, Riedl MS, Higgins L, Elde R. Identification of some lectin IB4 binding proteins in rat dorsal root ganglia. Neuroreport 2004, 15:1705-1709.
26. Gee MD, Lynn B, Cotsell B. Activity-dependent slowing of conduction velocity provides a method for identifying different functional classes of C-fibre in the rat saphenous nerve. Neuroscience 1996, 73:667-675.
27. Herzog RI, Cummins TR, Ghassemi F, Dib-Hajj SD, Waxman SG. Distinct repriming and closed-state inactivation kinetics of NaV1.6 and NaV1.7 sodium channels in mouse spinal sensory neurons. J Physiol 2003, 551:741-750.
28. McMahon SB. NGF as a mediator of inflammatory pain. Philos Trans R Soc Lond B Biol Sci 1996, 351:431-440.
29. Nassar MA, Stirling LC, Forlani G, Baker MD, Matthews EA, Dickenson AH, Wood JN. Nociceptor-specific gene deletion reveals a major role for NaV1.7 (PN1) in acute and inflammatory pain. Proc Natl Acad Sci U S A 2004, 101:12706-12711.
30. Neumcke B, Schwarz W, Stämpfli R. Modification of sodium inactivation in myelinated nerve by Anemonia toxin II and iodate. Analysis of current fluctuations and current relaxations. Biochim Biophys Acta 1980, 600:456-466.
31. Oliveira JS, Redaelli E, Zaharenko AJ, Cassulini RR, Konno K, Pimenta DC, Freitas JC, Clare JJ, Wanke E. Binding specificity of sea anemone toxins to NaV1.1-1.6 sodium channels: unexpected contributions from differences in the IV/S3-S4 outer loop. J Biol Chem 2004, 279:33323-33335.
32. Priestley JV, Michael GJ, Averill S, Liu M, Willmott N. Regulation of nociceptive neurons by nerve growth factor and glial cell line derived neurotrophic factor. Can J Physiol Pharmacol 2002, 80:495-505.
33. Rang HP, Ritchie JM. On the electrogenic sodium pump in mammalian non-myelinated nerve fibres and its activation by various external cations. J Physiol 1968, 196:183-221.
34. Raymond SA. Effects of nerve impulses on threshold of frog sciatic nerve fibres. J Physiol 1979, 290:273-303.
35. Reid G, Flonta M-L. Cold transduction by inhibition of a background potassium conductance in rat primary sensory neurones. Neurosci Lett 2001, 297:171-174.
36. Rogers JC, Qu Y, Tanada TN, Scheuer T, Catterall WA. Molecular determinants of high affinity binding of α-scorpion toxin and sea anemone toxin in the S3-S4 extracellular loop in domain IV of the Na+ channel α subunit. J Biol Chem 1996, 271:15950-15962.
37. Saab CY, Cummins TR, Dib-Hajj SD, Waxman SG. Molecular determinant of NaV1.8 sodium channel resistance to the venom from the scorpion Leiurus quinquestriatus hebraeus. Neurosci Lett 2002, 331:79-82.
38. Sangameswaran L, Delgado SG, Fish LM, Koch BD, Jakeman LB, Stewart GR, Sze P, Hunter JC, Eglen RM, Herman RC. Structure and function of a novel voltage-gated, tetrodotoxin-resistant sodium channel specific to sensory neurons. J Biol Chem 1996, 271:5953-5956.
39. Schmitt O, Schmidt H. Influence of calcium ions on the ionic currents of nodes of Ranvier treated with scorpion venom. Pflugers Arch 1972, 333:51-61.
40. Serra J, Campero M, Ochoa J, Bostock H. Activity-dependent slowing of conduction differentiates functional subtypes of C fibres innervating human skin. J Physiol 1999, 515:799-811.
41. Silverman JD, Kruger L. Selective neuronal glycoconjugate expression in sensory and autonomic ganglia: relation of lectin reactivity to peptide and enzyme markers. J Neurocytol 1990, 19:789-801.
42. Strassman AM, Raymond SA. Electrophysiological evidence for tetrodotoxin-resistant sodium channels in slowly conducting dural sensory fibres. J Neurophysiol 1999, 81:413-424.
43. Stucky CL, Lewin GR. Isolectin B4-positive and -negative nociceptors are functionally distinct. J Neurosci 1999, 19:6497-6505.
44. Vydyanathan A, Wu ZZ, Chen SR, Pan HL. A-type voltage-gated K+ currents influence firing properties of isolectin B4-positive but not isolectin B4-negative primary sensory neurons. J Neurophysiol 2005, 93:3401-3409.
45. Wang GK, Strichartz G. Kinetic analysis of the action of Leiurus scorpion α-toxin on ionic currents in myelinated nerve. J Gen Physiol 1985, 86:739-762.
46. Wanke E, Zaharenko AJ, Redaelli E, Schiavon E. Actions of sea anemone type 1 neurotoxins on voltage-gated sodium channel isoforms. Toxicon 2009, 54:1102-1111.
47. Westenbroek RE, Merrick DK, Catterall WA. Differential subcellular localization of the RI and RII Na+ channel subtypes in central neurons. Neuron 1989, 3:695-704.
48. Westenbroek RE, Noebels JL, Catterall WA. Elevated expression of type II Na+ channels in hypomyelinated axons of shiverer mouse brain. J Neurosci 1992, 12:2259-2267.
49. Wu CH, Narahashi T. Mechanism of action of novel marine neurotoxins on ion channels. Annu Rev Pharmacol Toxicol 1988, 28:141-161.
50. Wu ZZ, Pan HL. Tetrodotoxin-sensitive and -resistant Na+ channel currents in subsets of small sensory neurons of rats. Brain Res 2004, 1029:251-258.
51. Zimmermann K, Leffler A, Babes A, Cendan CM, Carr RW, Kobayashi J, Nau C, Wood JN, Reeh PW. Sensory neuron sodium channel NaV1.8 is essential for pain at low temperatures. Nature 2007, 447:855-858.