Neuropathic Nav1.3-mediated sensitization to P2X activation is regulated by protein kinase C

Molecular Pain

Volumn 7, Issue , 2011, Pages

  Mo, Gary ^a,b   Grant, Rebecca ^b   O'Donnell, Dajan ^b   Ragsdale, David S ^a   Cao, Chang Qing ^b   Séguéla, Philippe ^a  

^a MCGILL UNIVERSITY   (Canada)

^b ASTRAZENECA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALPHOSTIN C; PROTEIN KINASE C; PURINERGIC P2X RECEPTOR; SODIUM CHANNEL NAV1.3; STAUROSPORINE; ADENOSINE TRIPHOSPHATE; ALPHA,BETA METHYLENEADENOSINE TRIPHOSPHATE; ALPHA,BETA-METHYLENEADENOSINE 5'-TRIPHOSPHATE; DRUG DERIVATIVE; NAPHTHALENE DERIVATIVE; NERVE PROTEIN; SCN3A PROTEIN, RAT; SODIUM CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHO CELL; CONTROLLED STUDY; ENZYME REGULATION; HYPERSENSITIVITY; IN SITU HYBRIDIZATION; MALE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE INJURY; NERVE POTENTIAL; NEUROMODULATION; NEUROPATHIC PAIN; NONHUMAN; NUCLEOTIDE SEQUENCE; PATCH CLAMP; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SENSITIZATION; SODIUM CURRENT; SPINAL GANGLION; UPREGULATION; ACTION POTENTIAL; ANIMAL; CELL CULTURE; CRICETULUS; DRUG EFFECT; HAMSTER; HUMAN; METABOLISM; SPRAGUE DAWLEY RAT;

ACTION POTENTIALS; ADENOSINE TRIPHOSPHATE; ANIMALS; CELLS, CULTURED; CHO CELLS; CRICETINAE; CRICETULUS; GANGLIA, SPINAL; HUMANS; IN SITU HYBRIDIZATION; MALE; NAPHTHALENES; NERVE TISSUE PROTEINS; PATCH-CLAMP TECHNIQUES; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PURINERGIC P2X; SODIUM CHANNELS; STAUROSPORINE;

EID: 79751532255     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-7-14     Document Type: Article

References (47)

1. Dowd E, McQueen DS, Chessell IP, Humphrey PP. P2X receptor-mediated excitation of nociceptive afferents in the normal and arthritic rat knee joint. Br J Pharmacol 1998, 125:341-346. 10.1038/sj.bjp.0702080, 1565628, 9786507.
2. Rong W, Burnstock G, Spyer KM. P2X purinoceptor-mediated excitation of trigeminal lingual nerve terminals in an in vitro intra-arterially perfused rat tongue preparation. J Physiol 2000, 524(Pt 3):891-902. 10.1111/j.1469-7793.2000.00891.x, 2269894, 10790166.
3. Barclay J, Patel S, Dorn G, Wotherspoon G, Moffatt S, Eunson L, Abdel'al S, Natt F, Hall J, Winter J, et al. Functional downregulation of P2X3 receptor subunit in rat sensory neurons reveals a significant role in chronic neuropathic and inflammatory pain. J Neurosci 2002, 22:8139-8147.
4. Burnstock G, Wood JN. Purinergic receptors: their role in nociception and primary afferent neurotransmission. Curr Opin Neurobiol 1996, 6:526-532. 10.1016/S0959-4388(96)80060-2, 8794102.
5. Cockayne DA, Hamilton SG, Zhu QM, Dunn PM, Zhong Y, Novakovic S, Malmberg AB, Cain G, Berson A, Kassotakis L, et al. Urinary bladder hyporeflexia and reduced pain-related behaviour in P2X3-deficient mice. Nature 2000, 407:1011-1015. 10.1038/35039519, 11069181.
6. North RA, Verkhratsky A. Purinergic transmission in the central nervous system. Pflugers Arch 2006, 452:479-485. 10.1007/s00424-006-0060-y, 16688467.
7. Novakovic SD, Kassotakis LC, Oglesby IB, Smith JA, Eglen RM, Ford AP, Hunter JC. Immunocytochemical localization of P2X3 purinoceptors in sensory neurons in naive rats and following neuropathic injury. Pain 1999, 80:273-282. 10.1016/S0304-3959(98)00225-5, 10204740.
8. Xiang Z, Xiong Y, Yan N, Li X, Mao Y, Ni X, He C, LaMotte RH, Burnstock G, Sun J. Functional up-regulation of P2X 3 receptors in the chronically compressed dorsal root ganglion. Pain 2008, 140:23-34. 10.1016/j.pain.2008.07.006, 2667225, 18715715.
9. Bradbury EJ, Burnstock G, McMahon SB. The expression of P2X3 purinoreceptors in sensory neurons: effects of axotomy and glial-derived neurotrophic factor. Mol Cell Neurosci 1998, 12:256-268. 10.1006/mcne.1998.0719, 9828090.
10. Kage K, Niforatos W, Zhu CZ, Lynch KJ, Honore P, Jarvis MF. Alteration of dorsal root ganglion P2X3 receptor expression and function following spinal nerve ligation in the rat. Exp Brain Res 2002, 147:511-519. 10.1007/s00221-002-1263-x, 12444483.
11. Devor M. Sodium channels and mechanisms of neuropathic pain. J Pain 2006, 7:S3-S12. 10.1016/j.jpain.2005.09.006, 16426998.
12. Waxman SG, Kocsis JD, Black JA. Type III sodium channel mRNA is expressed in embryonic but not adult spinal sensory neurons, and is reexpressed following axotomy. J Neurophysiol 1994, 72:466-470. 2605356, 7965028.
13. Felts PA, Yokoyama S, Dib-Hajj S, Black JA, Waxman SG. Sodium channel alpha-subunit mRNAs I, II, III, NaG, Na6 and hNE (PN1): different expression patterns in developing rat nervous system. Brain Res Mol Brain Res 1997, 45:71-82. 10.1016/S0169-328X(96)00241-0, 9105672.
14. Chen Y, Yu FH, Surmeier DJ, Scheuer T, Catterall WA. Neuromodulation of Na+ channel slow inactivation via cAMP-dependent protein kinase and protein kinase C. Neuron 2006, 49:409-420. 10.1016/j.neuron.2006.01.009, 16446144.
15. Baker MD. Protein kinase C mediates up-regulation of tetrodotoxin-resistant, persistent Na+ current in rat and mouse sensory neurones. J Physiol 2005, 567:851-867. 10.1113/jphysiol.2005.089771, 1474230, 16002450.
16. Vijayaragavan K, Boutjdir M, Chahine M. Modulation of Nav1.7 and Nav1.8 peripheral nerve sodium channels by protein kinase A and protein kinase C. J Neurophysiol 2004, 91:1556-1569. 10.1152/jn.00676.2003, 14657190.
17. Cesare P, Dekker LV, Sardini A, Parker PJ, McNaughton PA. Specific involvement of PKC-epsilon in sensitization of the neuronal response to painful heat. Neuron 1999, 23:617-624. 10.1016/S0896-6273(00)80813-2, 10433272.
18. Malmberg AB, Chen C, Tonegawa S, Basbaum AI. Preserved acute pain and reduced neuropathic pain in mice lacking PKCgamma. Science 1997, 278:279-283. 10.1126/science.278.5336.279, 9323205.
19. Kim SH, Chung JM. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 1992, 50:355-363. 10.1016/0304-3959(92)90041-9, 1333581.
20. Meadows LS, Chen YH, Powell AJ, Clare JJ, Ragsdale DS. Functional modulation of human brain Nav1.3 sodium channels, expressed in mammalian cells, by auxiliary beta 1, beta 2 and beta 3 subunits. Neuroscience 2002, 114:745-753. 10.1016/S0306-4522(02)00242-7, 12220575.
21. 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, 389:816-824. 10.1038/39807, 9349813.
22. Velazquez KT, Mohammad H, Sweitzer SM. Protein kinase C in pain: involvement of multiple isoforms. Pharmacol Res 2007, 55:578-589. 10.1016/j.phrs.2007.04.006, 2140050, 17548207.
23. Yonezawa T, Kurata R, Kimura M, Inoko H. PKC delta and epsilon in drug targeting and therapeutics. Recent Pat DNA Gene Seq 2009, 3:96-101. 10.2174/187221509788654205, 19519579.
24. Plant TD, Zollner C, Kepura F, Mousa SS, Eichhorst J, Schaefer M, Furkert J, Stein C, Oksche A. Endothelin potentiates TRPV1 via ETA receptor-mediated activation of protein kinase C. Mol Pain 2007, 3:35. 10.1186/1744-8069-3-35, 2206006, 18001466.
25. Maruo K, Yamamoto H, Yamamoto S, Nagata T, Fujikawa H, Kanno T, Yaguchi T, Maruo S, Yoshiya S, Nishizaki T. Modulation of P2X receptors via adrenergic pathways in rat dorsal root ganglion neurons after sciatic nerve injury. Pain 2006, 120:106-112. 10.1016/j.pain.2005.10.016, 16360272.
26. Baron A, Deval E, Salinas M, Lingueglia E, Voilley N, Lazdunski M. Protein kinase C stimulates the acid-sensing ion channel ASIC2a via the PDZ domain-containing protein PICK1. J Biol Chem 2002, 277:50463-50468. 10.1074/jbc.M208848200, 12399460.
27. Dina OA, Barletta J, Chen X, Mutero A, Martin A, Messing RO, Levine JD. Key role for the epsilon isoform of protein kinase C in painful alcoholic neuropathy in the rat. J Neurosci 2000, 20:8614-8619.
28. Hua XY, Chen P, Yaksh TL. Inhibition of spinal protein kinase C reduces nerve injury-induced tactile allodynia in neuropathic rats. Neurosci Lett 1999, 276:99-102. 10.1016/S0304-3940(99)00818-6, 10624801.
29. Kobayashi E, Nakano H, Morimoto M, Tamaoki T. Calphostin C (UCN-1028C), a novel microbial compound, is a highly potent and specific inhibitor of protein kinase C. Biochem Biophys Res Commun 1989, 159:548-553. 10.1016/0006-291X(89)90028-4, 2467670.
30. Norcini M, Vivoli E, Galeotti N, Bianchi E, Bartolini A, Ghelardini C. Supraspinal role of protein kinase C in oxaliplatin-induced neuropathy in rat. Pain 2009, 146:141-147. 10.1016/j.pain.2009.07.017, 19683395.
31. Curia G, Aracri P, Colombo E, Scalmani P, Mantegazza M, Avanzini G, Franceschetti S. Phosphorylation of sodium channels mediated by protein kinase-C modulates inhibition by topiramate of tetrodotoxin-sensitive transient sodium current. Br J Pharmacol 2007, 150:792-797. 10.1038/sj.bjp.0707144, 2013870, 17279091.
32. Gold MS, Levine JD, Correa AM. Modulation of TTX-R INa by PKC and PKA and their role in PGE2-induced sensitization of rat sensory neurons in vitro. J Neurosci 1998, 18:10345-10355.
33. Wada A, Yanagita T, Yokoo H, Kobayashi H. Regulation of cell surface expression of voltage-dependent Nav1.7 sodium channels: mRNA stability and posttranscriptional control in adrenal chromaffin cells. Front Biosci 2004, 9:1954-1966. 10.2741/1314, 14977601.
34. Fukuoka T, Kobayashi K, Yamanaka H, Obata K, Dai Y, Noguchi K. Comparative study of the distribution of the alpha-subunits of voltage-gated sodium channels in normal and axotomized rat dorsal root ganglion neurons. J Comp Neurol 2008, 510:188-206. 10.1002/cne.21786, 18615542.
35. Kim CH, Oh Y, Chung JM, Chung K. The changes in expression of three subtypes of TTX sensitive sodium channels in sensory neurons after spinal nerve ligation. Brain Res Mol Brain Res 2001, 95:153-161. 10.1016/S0169-328X(01)00226-1, 11687287.
36. Boucher TJ, Okuse K, Bennett DL, Munson JB, Wood JN, McMahon SB. Potent analgesic effects of GDNF in neuropathic pain states. Science 2000, 290:124-127. 10.1126/science.290.5489.124, 11021795.
37. Siqueira SR, Alves B, Malpartida HM, Teixeira MJ, Siqueira JT. Abnormal expression of voltage-gated sodium channels Nav1.7, Nav1.3 and Nav1.8 in trigeminal neuralgia. Neuroscience 2009, 164:573-577. 10.1016/j.neuroscience.2009.08.037, 19699781.
38. Catterall WA, Goldin AL, Waxman SG. International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol Rev 2005, 57:397-409. 10.1124/pr.57.4.4, 16382098.
39. Isom LL, De Jongh KS, Patton DE, Reber BF, Offord J, Charbonneau H, Walsh K, Goldin AL, Catterall WA. Primary structure and functional expression of the beta 1 subunit of the rat brain sodium channel. Science 1992, 256:839-842. 10.1126/science.1375395, 1375395.
40. Shah BS, Stevens EB, Gonzalez MI, Bramwell S, Pinnock RD, Lee K, Dixon AK. beta3, a novel auxiliary subunit for the voltage-gated sodium channel, is expressed preferentially in sensory neurons and is upregulated in the chronic constriction injury model of neuropathic pain. Eur J Neurosci 2000, 12:3985-3990. 10.1046/j.1460-9568.2000.00294.x, 11069594.
41. Cummins TR, Aglieco F, Renganathan M, Herzog RI, Dib-Hajj SD, Waxman SG. Nav1.3 sodium channels: rapid repriming and slow closed-state inactivation display quantitative differences after expression in a mammalian cell line and in spinal sensory neurons. J Neurosci 2001, 21:5952-5961.
42. Cusdin FS, Nietlispach D, Maman J, Dale TJ, Powell AJ, Clare JJ, Jackson AP. The sodium channel {beta}3-subunit induces multiphasic gating in NaV1.3 and affects fast inactivation via distinct intracellular regions. J Biol Chem 2010, 285:33404-33412. 10.1074/jbc.M110.114058, 20675377.
43. Hains BC, Klein JP, Saab CY, Craner MJ, Black JA, Waxman SG. Upregulation of sodium channel Nav1.3 and functional involvement in neuronal hyperexcitability associated with central neuropathic pain after spinal cord injury. J Neurosci 2003, 23:8881-8892.
44. Hains BC, Saab CY, Klein JP, Craner MJ, Waxman SG. Altered sodium channel expression in second-order spinal sensory neurons contributes to pain after peripheral nerve injury. J Neurosci 2004, 24:4832-4839. 10.1523/JNEUROSCI.0300-04.2004, 15152043.
45. Lindia JA, Kohler MG, Martin WJ, Abbadie C. Relationship between sodium channel Nav1.3 expression and neuropathic pain behavior in rats. Pain 2005, 117:145-153. 10.1016/j.pain.2005.05.027, 16061326.
46. Nassar MA, Baker MD, Levato A, Ingram R, Mallucci G, McMahon SB, Wood JN. Nerve injury induces robust allodynia and ectopic discharges in Nav1.3 null mutant mice. Mol Pain 2006, 2:33. 10.1186/1744-8069-2-33, 1630424, 17052333.
47. Hudmon A, Choi JS, Tyrrell L, Black JA, Rush AM, Waxman SG, Dib-Hajj SD. Phosphorylation of sodium channel Nav1.8 by p38 mitogen-activated protein kinase increases current density in dorsal root ganglion neurons. J Neurosci 2008, 28:3190-3201. 10.1523/JNEUROSCI.4403-07.2008, 18354022.