Functional upregulation of Nav1.8 sodium channels on the membrane of dorsal root ganglia neurons contributes to the development of cancer-induced bone pain

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Liu, Xiao Dan ^a,b   Yang, Jing Jing ^a   Fang, Dong ^a   Cai, Jie ^a,b   Wan, You ^b   Xing, Guo Gang ^a,b,c  

^a PEKING UNIVERSITY   (China)

^b PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^c BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

A 803467; SODIUM CHANNEL BLOCKING AGENT; SODIUM CHANNEL NAV1.8; UNCLASSIFIED DRUG; ANILINE DERIVATIVE; FURAN DERIVATIVE; SCN10A PROTEIN, RAT;

ACTION POTENTIAL; ADULT; ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE CANCER; BONE PAIN; CELL BEHAVIOR ASSAY; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEMALE; HYPERALGESIA; NERVE CELL EXCITABILITY; NONHUMAN; PROTEIN EXPRESSION; QUALITY OF LIFE; RAT; SPINAL GANGLION; UPREGULATION; WESTERN BLOTTING; ANIMAL; BONE TUMOR; CELL MEMBRANE; COMPLICATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; NERVE CELL; PAIN; PATHOLOGY; SPRAGUE DAWLEY RAT; TUMOR CELL LINE;

RATTUS;

ANILINE COMPOUNDS; ANIMALS; BONE NEOPLASMS; CELL LINE, TUMOR; CELL MEMBRANE; ELECTROPHYSIOLOGICAL PROCESSES; FEMALE; FURANS; GANGLIA, SPINAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HYPERALGESIA; NAV1.8 VOLTAGE-GATED SODIUM CHANNEL; NEURONS; PAIN; RATS; RATS, SPRAGUE-DAWLEY; SODIUM CHANNEL BLOCKERS; UP-REGULATION;

EID: 84918564868     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114623     Document Type: Article

References (40)

1. Jimenez-Andrade JM, Mantyh WG, Bloom AP, Ferng AS, Geffre CP, et al. (2010) Bone cancer pain. Ann N Y Acad Sci 1198: 173-181.
2. Zhao J, Pan HL, Li TT, Zhang YQ, Wei JY, et al. (2010) The sensitization of peripheral C-fibers to lysophosphatidic acid in bone cancer pain. Life Sci 87: 120-125.
3. Zheng Q, Fang D, Cai J, Wan Y, Han JS, et al. (2012) Enhanced excitability of small dorsal root ganglion neurons in rats with bone cancer pain. Mol Pain 8: 24.
4. Dib-Hajj SD, Cummins TR, Black JA, Waxman SG (2010) Sodium Channels in Normal and Pathological Pain. Annu.Rev.Neurosci. 33: 325-347.
5. Rugiero F, Mistry M, Sage D, Black JA, Waxman SG, et al. (2003) Selective expression of a persistent tetrodotoxin-resistant Na+ current and NaV1.9 subunit in myenteric sensory neurons. J Neurosci 23: 2715-2725.
6. Akopian AN, Sivilotti L, Wood JN (1996) A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 379: 257-262.
7. Akopian AN, Souslova V, England S, Okuse K, Ogata N, et al. (1999) The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat Neurosci 2: 541-548.
8. Blair NT, Bean BP (2002) Roles of tetrodotoxin (TTX)-sensitive Na+ current, TTX-resistant Na+ current, and Ca2+ current in the action potentials of nociceptive sensory neurons. J Neurosci 22: 10277-10290.
9. Renganathan M, Cummins TR, Waxman SG (2001) Contribution of Na(v)1.8 sodium channels to action potential electrogenesis in DRG neurons. J Neurophysiol 86: 629-640.
10. Qiu F, Jiang Y, Zhang H, Liu Y, Mi W (2012) Increased expression of tetrodotoxin-resistant sodium channels Nav1.8 and Nav1.9 within dorsal root ganglia in a rat model of bone cancer pain. Neurosci Lett 512: 61-66.
11. Zimmermann M (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16: 109-110.
12. Medhurst SJ, Walker K, Bowes M, Kidd BL, Glatt M, et al. (2002) A rat model of bone cancer pain. Pain 96: 129-140.
13. Zheng Q, Fang D, Liu M, Cai J, Wan Y, et al. (2013) Suppression of KCNQ/M (Kv7) potassium channels in dorsal root ganglion neurons contributes to the development of bone cancer pain in a rat model. Pain 154: 434-448.
14. Djouhri L, Fang X, Okuse K, Wood JN, Berry CM, et al. (2003) The TTX-resistant sodium channel Nav1.8 (SNS/PN3): expression and correlation with membrane properties in rat nociceptive primary afferent neurons. J Physiol 550: 739-752.
15. Fang X, Djouhri L, Black JA, Dib-Hajj SD, Waxman SG, et al. (2002) The presence and role of the tetrodotoxin-resistant sodium channel Na(v)1.9 (NaN) in nociceptive primary afferent neurons. J Neurosci 22: 7425-7433.
16. Rush AM, Waxman SG (2004) PGE2 increases the tetrodotoxin-resistant Nav1.9 sodium current in mouse DRG neurons via G-proteins. Brain Res 1023: 264-271.
17. Berta T, Poirot O, Pertin M, Ji RR, Kellenberger S, et al. (2008) Transcriptional and functional profiles of voltage-gated Na(+) channels in injured and non-injured DRG neurons in the SNI model of neuropathic pain. Mol Cell Neurosci 37: 196-208.
18. Liu M, Yang H, Fang D, Yang JJ, Cai J, et al. (2013) Upregulation of P2X3 receptors by neuronal calcium sensor protein VILIP-1 in dorsal root ganglions contributes to the bone cancer pain in rats. Pain 154: 1551-1568.
19. Black JA, Liu S, Tanaka M, Cummins TR, Waxman SG (2004) Changes in the expression of tetrodotoxin-sensitive sodium channels within dorsal root ganglia neurons in inflammatory pain. Pain 108: 237-247.
20. Qu XX, Cai J, Li MJ, Chi YN, Liao FF, et al. (2009) Role of the spinal cord NR2B-containing NMDA receptors in the development of neuropathic pain. Exp Neurol 215: 298-307.
21. Geng SJ, Liao FF, Dang WH, Ding X, Liu XD, et al. (2010) Contribution of the spinal cord BDNF to the development of neuropathic pain by activation of the NR2B-containing NMDA receptors in rats with spinal nerve ligation. Exp Neurol 222: 256-266.
22. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J.Neurosci.Methods 53: 55-63.
23. Dixon WJ (1980) Efficient analysis of experimental observations. Annu.Rev.Pharmacol. Toxicol 20: 441-462.
24. Rivlin AS, Tator CH (1977) Objective clinical assessment of motor function after experimental spinal cord injury in the rat. J.Neurosurg. 47: 577-581.
25. Chen X, Pang RP, Shen KF, Zimmermann M, Xin WJ, et al. (2011) TNF-alpha enhances the currents of voltage gated sodium channels in uninjured dorsal root ganglion neurons following motor nerve injury. Exp Neurol 227: 279-286.
26. Jarvis MF, Honore P, Shieh CC, Chapman M, Joshi S, 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 U S A 104: 8520-8525.
27. McGaraughty S, Chu KL, Scanio MJ, Kort ME, Faltynek CR, et al. (2008) A selective Nav1.8 sodium channel blocker, A-803467 [5-(4-chlorophenyl-N-(3,5-dimethoxyphenyl) furan-2-carboxamide], attenuates spinal neuronal activity in neuropathic rats. J Pharmacol Exp Ther 324: 1204-1211.
28. Brouwer BA, Merkies IS, Gerrits MM, Waxman SG, Hoeijmakers JG, et al. (2014) Painful neuropathies: the emerging role of sodium channelopathies. J.Peripher.Nerv.Syst. 19: 53-65.
29. Momin A, Wood JN (2008) Sensory neuron voltage-gated sodium channels as analgesic drug targets. Curr.Opin.Neurobiol. 18: 383-388.
30. Joshi SK, Honore P, Hernandez G, Schmidt R, Gomtsyan A, et al. (2009) Additive antinociceptive effects of the selective Nav1.8 blocker A-803467 and selective TRPV1 antagonists in rat inflammatory and neuropathic pain models. J Pain 10: 306-315.
31. Joshi SK, Mikusa JP, Hernandez G, Baker S, Shieh CC, et al. (2006) Involvement of the TTX-resistant sodium channel Nav 1.8 in inflammatory and neuropathic, but not post-operative, pain states. Pain 123: 75-82.
32. Miao XR, Gao XF, Wu JX, Lu ZJ, Huang ZX, et al. (2010) Bilateral downregulation of Nav1.8 in dorsal root ganglia of rats with bone cancer pain induced by inoculation with Walker 256 breast tumor cells. BMC Cancer 10: 216.
33. Minett MS, Falk S, Santana-Varela S, Bogdanov YD, Nassar MA, et al. (2014) Pain without nociceptors? Nav1.7-independent pain mechanisms. Cell Rep 6: 301-312.
34. Dib-Hajj SD, Binshtok AM, Cummins TR, Jarvis MF, Samad T, et al. (2009) Voltage-gated sodium channels in pain states: role in pathophysiology and targets for treatment. Brain Res.Rev. 60: 65-83.
35. Moldovan M, Alvarez S, Romer RM, Krarup C (2013) Axonal voltage-gated ion channels as pharmacological targets for pain. Eur.J.Pharmacol. 708: 105-112.
36. Khasar SG, Gold MS, Levine JD (1998) A tetrodotoxin-resistant sodium current mediates inflammatory pain in the rat. Neurosci.Lett. 256: 17-20.
37. Lai J, Gold MS, Kim CS, Bian D, Ossipov MH, et al. (2002) Inhibition of neuropathic pain by decreased expression of the tetrodotoxin-resistant sodium channel, NaV1.8. Pain. 95: 143-152.
38. Dong XW, Goregoaker S, Engler H, Zhou X, Mark L, et al. (2007) Small interfering RNA-mediated selective knockdown of Na(V)1.8 tetrodotoxin-resistant sodium channel reverses mechanical allodynia in neuropathic rats. Neuroscience 146: 812-821.
39. Matsutomi T, Nakamoto C, Zheng T, Kakimura J, Ogata N (2006) Multiple types of Na(+) currents mediate action potential electrogenesis in small neurons of mouse dorsal root ganglia. Pflugers Arch 453: 83-96.
40. Zimmermann K, Leffler A, Babes A, Cendan CM, Carr RW, et al. (2007) Sensory neuron sodium channel Nav1.8 is essential for pain at low temperatures. Nature 447: 855-858.