Involvement of peripheral adenosine 5′-triphosphate and P2X purinoceptor in pain-related behavior produced by orthotopic melanoma inoculation in mice

European Journal of Neuroscience

Volumn 31, Issue 9, 2010, Pages 1629-1636

  Fujita, Masahide ^a   Andoh, Tsugunobu ^a   Sasaki, Atsushi ^a   Saiki, Ikuo ^a   Kuraishi, Yasushi ^a  

^a UNIVERSITY OF TOYAMA   (Japan)

Author keywords

Cancer pain; Dorsal root ganglion; Licking behavior; Microdialysis; Tibial nerve

Indexed keywords

2',3' O (2,4,6 TRINITROPHENYL)ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; PERIPHERIN; PURINERGIC P2X3 RECEPTOR; PURINERGIC RECEPTOR BLOCKING AGENT; PYRIDOXAL PHOSPHATE 6 AZOPHENYL 2',4' DISULFONIC ACID; SURAMIN; UNCLASSIFIED DRUG; P2RX3 PROTEIN, MOUSE; PURINERGIC P2 RECEPTOR; PURINERGIC P2 RECEPTOR ANTAGONIST; PURINERGIC P2X RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER PAIN; CONTROLLED STUDY; DRUG DOSE COMPARISON; HINDLIMB; LICKING; MALE; MELANOMA; MOUSE; NOCICEPTION; NONHUMAN; PAIN ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; ROTAROD TEST; SPINAL GANGLION; TIBIAL NERVE; 3T3 CELL LINE; ACTION POTENTIAL; ANIMAL; ANIMAL BEHAVIOR; BREAST TUMOR; C57BL MOUSE; COMPLICATION; DRUG EFFECTS; FEMALE; FIBROBLAST; LUNG TUMOR; MELANOMA, EXPERIMENTAL; METABOLISM; NERVE CELL; PAIN; PATHOPHYSIOLOGY; PHYSIOLOGY; SKIN NEOPLASMS; TUMOR CELL LINE;

ACTION POTENTIALS; ADENOSINE TRIPHOSPHATE; ANIMALS; BEHAVIOR, ANIMAL; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; FIBROBLASTS; GANGLIA, SPINAL; LUNG NEOPLASMS; MALE; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; NEURONS; NIH 3T3 CELLS; PAIN; PURINERGIC P2 RECEPTOR ANTAGONISTS; RECEPTORS, PURINERGIC P2; RECEPTORS, PURINERGIC P2X; RECEPTORS, PURINERGIC P2X3; SKIN NEOPLASMS; TIBIAL NERVE;

EID: 77951780827     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07185.x     Document Type: Article

References (54)

1. Baiou, D., Santha, P., Avelino, A., Charrua, A., Bacskai, T., Matesz, K., Cruz, F. Nagy, I. (2007) Neurochemical characterization of insulin receptor-expressing primary sensory neurons in wild-type and vanilloid type 1 transient receptor potential receptor knockout mice. J. Comp. Neurol., 503, 334 347.
2. Bleehen, T. (1978) The effects of adenine nucleotides on cutaneous afferent nerve activity. Br. J. Pharmacol., 62, 573 577.
3. Bleehen, T. Keele, C.A. (1977) Observation on the algogenic actions of adenosine compounds on the human blister base preparation. Pain, 3, 367 377.
4. Bodin, P. Burnstock, G. (1998) Increase release of ATP from endothelial cells during acute inflammation. Inflamm. Res., 47, 351 354.
5. Bourquin, A.F., Suveges, M., Pertin, M., Gilliard, N., Sardy, S., Davison, A.C., Spahn, D.R. Decosterd, I. (2006) Assessment and analysis of mechanical allodynia-like behavior induced by spared nerve injury (SNI) in the mouse. Pain, 122, 14.e1 14.e14.
6. Broom, D.C., Matson, D.J., Bradshaw, E., Buck, M.E., Meade, R., Coombs, S., Matchett, M., Ford, K.K., Yu, W., Yuan, J., Sun, S.H., Ochoa, R., Krause, J.E., Wustrow, D.J. Cortright, D.N. (2008) Characterization of N-(adamantan-1-ylmethyl)-5-[(3R- amino-pyrrolidin-1-yl)methyl]-2-chloro-ben zamide, a P2X7 antagonist in animal models of pain and inflammation. J. Pharmacol. Exp. Ther., 327, 620 633.
7. Burnstock, G. (1996) A unifying purinergic hypothesis for the initiation of pain. Lancet, 347, 1604 1605.
8. Burnstock, G. (2006) Historical review: ATP as a neurotransmitter. Trends Pharmacol. Sci., 27, 166 176.
9. Chen, Y., Li, G.W., Wang, C., Gu, Y. Haung, L.M. (2005) Mechanisms underlying enhanced P2X receptor-mediated responses in the neuropathic pain state. Pain, 119, 38 48.
10. Chen, Y., Zhang, X., Wang, C., Li, G.W., Gu, Y. Huang, L.M. (2008) Activation of P2X7 receptors in glial satellite cells reduces pain through downregulation of P2X3 receptors in nociceptive neurons. Proc. Natl Acad. Sci. USA, 105, 16773 16778.
11. Chizhmakov, I., Yudin, Y., Mamenko, N., Prudnikov, I., Tamarova, Z. Krishtal, O. (2005) Opioids inhibit purinergic nociceptors in the sensory neurons and fibres of rat via a G protein-dependent mechanism. Neuropharmacology, 48, 639 647.
12. Cockayne, D.A., Dunn, P.M., Zhong, Y., Rong, W., Hamilton, S.G., Knight, G.E., Ruan, H.Z., Ma, B., Yip, P., Nunn, P., McMahon, S.B., Burnstock, G. Ford, A.P. (2005) P2X2 knockout mice and P2X2/P2X3 double knockout mice reveal a role for the P2X2 receptor subunit in mediating multiple sensory effects of ATP. J. Physiol., 567, 621 639.
13. Collo, G., North, R.A., Kawashima, E., Merlo-Pich, E., Neidhart, S., Surprenant, A. Buell, G. (1996) Cloning of P2X5 and P2X6 receptors and the distribution and properties of an extended family of ATP-gated ion channels. J. Neurosci., 16, 2495 2507.
14. Cook, S.P. McCleskey, E.W. (2002) Cell damage excites nociceptors through release of cytosolic ATP. Pain, 95, 41 47.
15. Fujita, M., Andoh, T., Saiki, I. Kuraishi, Y. (2008) Involvement of endothelin and ETA endothelin receptor in mechanical allodynia in mice given orthotopic melanoma inoculation. J. Pharmacol. Sci., 106, 257 263.
16. Fujita, M., Andoh, T., Ohashi, K., Akira, A., Saiki, I. Kuraishi, Y. (2009) Roles of kinin B1 and B2 receptors in skin cancer pain produced by orthotopic melanoma inoculation in mice. Eur. J. Pain. Doi:.
17. Gilchrist, L.S., Cain, D.M., Harding-Rose, C., Kov, A.N., Wendelschafer-Crabb, G., Kennedy, W.R. Simone, D.A. (2005) Re-organization of P2X3 receptor localization on epidermal nerve fibers in a murine model of cancer pain. Brain Res., 1044, 197 205.
18. Goldstein, M.E., House, S.B. Gainer, H. (1991) NF-L and peripherin immunoreactivities define distinct classes of rat sensory ganglion cells. J. Neurosci. Res., 30, 92 104.
19. Hald, A., Nedergaard, S., Hansen, R.R., Ding, M. Heegaard, A.M. (2009) Differential activation of spinal cord glial cells in murine models of neuropathic and cancer pain. Eur. J. Pain, 13, 138 145.
20. Hamilton, S.G., Wade, A. McMahon, S.B. (1999) The effects of inflammation and inflammatory mediators on nociceptive behavior induced by ATP analogues in the rat. Br. J. Pharmacol., 126, 326 332.
21. Hamilton, S.G., Warburton, J., Bhattacharjee, A., Ward, J. McMahon, S.B. (2000) ATP in human skin elicits a dose-related pain response which is potentiated under conditions of hyperalgesia. Brain, 123, 1238 1246.
22. Jarvis, M.F., Burgard, E.C., McGaraughty, S., Honore, P., Lynch, K., Brennan, T.J., Subieta, A., Van Biesen, T., Cartmell, J., Bianchi, B., Niforatos, W., Kage, K., Yu, H., Mikusa, J., Wismer, C.T., Zhu, C.Z., Chu, K., Lee, C.H., Stewart, A.O., Polakowski, J., Cox, B.F., Kowaluk, E., Williams, M., Sullivan, J. Faltynek, C. (2002) A-317491, a novel potent and selective non-nucleotide antagonist of P2X3 and P2X2/3 receptors, reduces chronic inflammatory and neuropathic pain in the rat. Proc. Natl Acad. Sci. USA, 24, 17179 17184.
23. Khakh, B.S., Burnstock, G., Kennedy, C., King, B.F., North, R.A., Seguela, P., Voigt, M. Humphrey, P.P. (2001) International union of pharmacology. XXIV. Current status of the nomenclature and properties of P2X receptors and their subunits. Pharmacol. Rev., 53, 107 118.
24. Khasabova, I.A., Stucky, C.L., Harding-Rose, C., Eikmeier, L., Beitz, A.J., Coicou, L.G., Hanson, A.E., Simone, D.A. Seybold, V.S. (2007) Chemical interactions between fibrosarcoma cancer cells and sensory neurons contribute to cancer pain. J. Neurosci., 19, 10289 10298.
25. Kobayashi, K., Fukuoka, T., Yamanaka, H., Dai, Y., Obata, K., Tokunaga, A. Noguchi, K. (2005) Differential expression patterns of mRNAs for P2X receptor subunits in neurochemically characterized dorsal root ganglion neurons in the rat. J. Comp. Neurol., 481, 377 390.
26. Koizumi, S., Fujishita, K., Inoue, K., Shigemoto-Mogami, Y., Tsuda, M. Inoue, K. (2004) Ca2+ waves in keratinocytes are transmitted to sensory neurons: the involvement of extracellular ATP and P2Y2 receptor activation. Biochem. J., 380, 329 338.
27. Lewis, C., Neidhart, S., Holy, C., North, R.A., Buell, G. Surprenant, A. (1995) Coexpression of P2X2 and P2X3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature, 377, 432 435.
28. Maehara, Y., Kusumoto, H., Anai, H., Kusumoto, T. Sugimachi, K. (1987) Human tumor tissues have higher ATP contents than normal tissues. Clin. Chim. Acta, 167, 341 344.
29. McGaraughty, S., Wismer, C.T., Zhu, C.Z., Mikusa, J., Honore, P., Chu, K.L., Lee, C.H., Faltynek, C.R. Jarvis, M.F. (2003) Effect of A-317491, a novel and selective P2X3/P2X2/3 receptor antagonist, on neuropathic, inflammatory and chemogenic nociception following intrathecal and intraplantar administration. Br. J. Pharmacol., 140, 1381 1388.
30. Omori, Y., Kagaya, K., Enomoto, R., Sasaki, A., Andoh, T., Nojima, H., Takahata, H. Kuraishi, Y. (2009) A mouse model of sural nerve injury-induced neuropathy: gabapentin inhibits pain-related behaviors and the hyperactivity of wide-dynamic range neurons in the dorsal horn. J. Pharmacol. Sci., 109, 532 539.
31. Portenoy, R.K. Lesage, P. (1999) Management of cancer pain. Lancet, 353, 1695 1700.
32. Sanderson, L., Khan, A. Thomas, S. (2007) Distribution of suramin, an antitrypanosomal drug, across the blood-brain and blood-cerebrospinal fluid interfaces in wild-type and P-glycoprotein transporter-deficient mice. Antimicrob. Agents Chemother., 51, 3136 3146.
33. Sasamura, T., Nakamura, S., Iida, Y., Fujii, H., Murata, J., Saiki, I., Nojima, H. Kuraishi, Y. (2002) Morphine analgesia suppresses tumor growth and metastasis in a mouse model of cancer pain induced by orthotopic tumor inoculation. Eur. J. Pharmacol., 441, 185 191.
34. Schmidt, B.L., Pickering, V., Liu, S., Quang, P., Dolan, J., Connelly, S.T. Jordan, R.C. (2007) Peripheral endothelin A receptor antagonism attenuates carcinoma-induced pain. Eur. J. Pain, 11, 406 414.
35. Seino, D., Tokunaga, A., Tachibana, T., Yoshiya, S., Dai, Y., Obata, K., Yamanaka, H., Kobayashi, K. Noguchi, K. (2006) The role of ERK signaling and the P2X receptor on mechanical pain evoked by movement of inflamed knee joint. Pain, 123, 193 203.
36. Sevcik, M.A., Ghilardi, J.R., Halvorson, K.G., Lindsay, T.H., Kubota, K. Mantyh, P.W. (2005a) Analgesic efficacy of bradykinin B1 antagonists in a murine bone cancer pain model. J Pain, 6, 771 775.
37. Sevcik, M.A., Ghilardi, J.R., Peters, C.M., Lindsay, T.H., Halvorson, K.G., Jonas, B.M., Kubota, K., Kuskowski, M.A., Boustany, L., Shelton, D.L. Mantyh, P.W. (2005b) Anti-NGF therapy profoundly reduces bone cancer pain and the accompanying increase in markers of peripheral and central sensitization. Pain, 115, 128 141.
38. Siems, W.G., Grune, T., Schmidt, H., Tikhonov, Y.V. Pimenov, A.M. (1993) Purine nucleotide levels in host tissues of Ehrlich ascites tumor-bearing mice in different growth phases of the tumor. Cancer Res., 53, 5143 5147.
39. Souslova, V., Cesare, P., Ding, Y., Akopian, A.N., Stanfa, L., Suzuki, R., Carpenter, K., Dickenson, A., Boyce, S., Hill, R., Nebenuis-Oosthuizen, D., Smith, A.J., Kidd, E.J. Wood, J.N. (2000) Warm-coding deficits and aberrant inflammatory pain in mice lacking P2X3 receptors. Nature, 407, 1015 1017.
40. Tsuda, M., Shigemoto-Mogami, Y., Ueno, S., Koizumi, S., Ueda, H., Iwanaga, T. Inoue, K. (2002) Downregulation of P2X3 receptor-dependent sensory functions in A/J inbred mouse strain. Eur. J. Neurosci., 15, 1444 1450.
41. Tsuda, M., Shigemoto-Mogami, Y., Koizumi, S., Mizokoshi, A., kohsaku, S., Salter, M.W. Inoue, K. (2003) P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature, 424, 778 783.
42. Tsuda, M., Kuboyama, K., Inoue, T., Nagata, K., Tozaki-Saitoh, H. Inoue, K. (2009) Behavioral phenotypes of mice lacking purinergic P2X4 receptors in acute and chronic pain assays. Mol. Pain, 5, 28 34.
43. Tsuzuki, K., Kondo, E., Fukuoka, T., Yi, D., Tsujino, H., Sakagami, M. Noguchi, K. (2001) Differential regulation of P2X3 mRNA expression by peripheral nerve injury in intact and injured neurons in the rat sensory ganglia. Pain, 91, 351 360.
44. Ueno, S., Tsuda, M., Iwanaga, T. Inoue, K. (1999) Cell type-specific ATP-activated responses in rat dorsal root ganglion neurons. Br. J. Pharmacol., 126, 429 436.
45. Wacnik, P.W., Eikmeier, L.J., Ruggles, T.R., Ramnaraine, M.L., Walcheck, B.K., Beitz, A.J. Wilcox, G.L. (2001) Functional interactions between tumor and peripheral nerve: morphology, algogen identification, and behavioral characterization of a new murine model of cancer pain. J. Neurosci., 21, 9355 9366.
46. Wacnik, P.W., Baker, C.M., Herron, M.J., Kren, B.T., Blazar, B.R., Wilcox, G.L., Hordinsky, M.K., Neitz, A.J. Ericson, M.E. (2005a) Tumor-induced mechanical hyperalgesia involves CGRP receptors and altered innervation and vascularization of DsRed2 fluorescent hindpaw tumors. Pain, 115, 95 106.
47. Wacnik, P.W., Eikmeier, L.J., Simone, D.A., Wilcox, G.L. Beitz, A.J. (2005b) Nociceptive characteristics of tumor necrosis factor-α in naive and tumor-bearing mice. Neuroscience, 132, 479 491.
48. Wang, Y., Mackes, J., Chan, S., Haughey, N.J., Guo, Z., Ouyang, X., Furukawa, K., Ingram, D.K. Mattson, M.P. (2006) Impaired long-term depression in P2X3 deficient mice is not associated with a spatial learning deficit. J. Neurochem., 99, 1425 1434.
49. Wirkner, K., Sperlagh, B. Illes, P. (2007) P2X3 receptor involvement in pain states. Mol. Neurobiol., 36, 165 183.
50. Xu, G.Y. Huang, L.Y. (2004) Ca2+/calmodulin-dependent protein kinase II potentiates ATP responses by promoting trafficking of P2X receptors. Proc. Natl Acad. Sci. USA, 101, 11868 11873.
51. Xu, G.Y. Huanq, L.Y. (2002) Peripheral inflammation sensitizes P2X receptor-mediated responses in rat dorsal root ganglion neurons. J. Neurosci., 22, 93 102.
52. Zhang, H., Sasamura, T., Iida, Y., Nojima, H., Murata, J., Saiki, I. Kuraishi, Y. (2001) Algogenic effects of the extract of tumor mass isolated from mice with orthotopic inoculation of melanoma cell. Pain Res., 16, 43 49.
53. Zhang, H., Iida, Y., Andoh, T., Nojima, H., Murata, J., Saiki, I. Kuraishi, Y. (2003) Mechanical hypersensitivity and alterations in cutaneous nerve fibers in a mouse model of skin cancer pain. J. Pharmacol. Sci., 91, 167 170.
54. Zimmermann, M. (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain, 16, 109 110.