Involvement of TRPV1 in Nociceptive Behavior in a Rat Model of Cancer Pain

Journal of Pain

Volumn 9, Issue 8, 2008, Pages 687-699

  Shinoda, Masamichi ^a   Ogino, Akina ^a   Ozaki, Noriyuki ^a   Urano, Hiroko ^a,b   Hironaka, Katsunori ^a   Yasui, Masaya ^a   Sugiura, Yasuo ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b MIE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

mechanical allodynia; spontaneous nocifensive behavior; thermal hyperalgesia; TRPV1; TRPV2

Indexed keywords

CAPSAZEPINE; MORPHINE; RUTHENIUM RED; TRANSIENT RECEPTOR POTENTIAL CHANNEL; VANILLOID RECEPTOR 1; VANILLOID RECEPTOR 2;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER PAIN; CONTROLLED STUDY; DRUG ADMINISTRATION ROUTE; DRUG EFFECT; DRUG MECHANISM; HYPERALGESIA; INTRAPLANTAR DRUG ADMINISTRATION; MALE; NERVE CELL; NOCICEPTION; NONHUMAN; RAT; SPINAL GANGLION; SQUAMOUS CELL CARCINOMA; TUMOR GROWTH;

ANALGESICS, OPIOID; ANIMALS; BEHAVIOR, ANIMAL; CAPSAICIN; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; FOOT DISEASES; GANGLIA, SPINAL; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; INJECTIONS, INTRAPERITONEAL; INJECTIONS, SUBCUTANEOUS; MALE; MORPHINE; NEOPLASMS, EXPERIMENTAL; NOCICEPTORS; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; RATS; RATS, INBRED F344; RUTHENIUM RED; TRPV CATION CHANNELS;

EID: 47549101002     PISSN: 15265900     EISSN: 15288447     Source Type: Journal    
DOI: 10.1016/j.jpain.2008.02.007     Document Type: Article

References (56)

1. Ahluwalia J., Rang H., and Nagy I. The putative role of vanilloid receptor-like protein-1 in mediating high threshold noxious heat-sensitivity in rat cultured primary sensory neurons. Eur J Neurosci 16 (2002) 1483-1489
2. Amaya F., Oh-hashi K., Naruse Y., Iijima N., Ueda M., Shimosato G., Tominaga M., Tanaka Y., and Tanaka M. Local inflammation increases vanilloid receptor 1 expression within distinct subgroups of DRG neurons. Brain Res 963 (2003) 190-196
3. Amaya F., Shimosato G., Nagano M., Ueda M., Hashimoto S., Tanaka Y., Suzuki H., and Tanaka M. NGF and GDNF differentially regulate TRPV1 expression that contributes to development of inflammatory thermal hyperalgesia. Eur J Neurosci 20 (2004) 2303-2310
4. Asai H., Ozaki N., Shinoda M., Nagamine K., Tohnai I., Ueda M., and Sugiura Y. Heat and mechanical hyperalgesia in mice model of cancer pain. Pain 117 (2005) 19-29
5. Breese N.M., George A.C., Pauers L.E., and Stucky C.L. Peripheral inflammation selectively increases TRPV1 function in IB4-positive sensory neurons from adult mouse. Pain 115 (2005) 37-49
6. Bryant J.A., Finn R.S., Slamon D.J., Cloughesy T.F., and Charles A.C. EGF activates intracellular and intercellular calcium signaling by distinct pathways in tumor cells. Cancer Biol Ther 3 (2004) 1243-1249
7. Caterina M.J., Rosen T.A., Tominaga M., Brake A.J., and Julius D. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398 (1999) 436-441
8. Chung M.K., Lee H., and Caterina M.J. Warm temperatures activate TRPV4 in mouse 308 keratinocytes. J Biol Chem 278 (2003) 32037-32046
9. Chung M.K., Lee H., Mizuno A., Suzuki M., and Caterina M.J. 2-aminoethoxydiphenyl borate activates and sensitizes the heat-gated ion channel TRPV3. J Neurosci 24 (2004) 5177-5182
10. Chung M.K., Lee H., Mizuno A., Suzuki M., and Caterina M.J. TRPV3 and TRPV4 mediate warmth-evoked currents in primary mouse keratinocytes. J Biol Chem 279 (2004) 21569-21575
11. Cui M., Honore P., Zhong C., Gauvin D., Mikusa J., Hernandez G., Chandran P., Gomtsyan A., Brown B., Bayburt E.K., Marsh K., Bianchi B., McDonald H., Niforatos W., Neelands T.R., Moreland R.B., Decker M.W., Lee C.H., Sullivan J.P., and Faltynek C.R. TRPV1 receptors in the CNS play a key role in broad-spectrum analgesia of TRPV1 antagonists. J Neurosci 26 (2006) 9385-9393
12. Fukuoka T., Tokunaga A., Tachibana T., Dai Y., Yamanaka H., and Noguchi K. VR1, but not P2X(3), increases in the spared L4 DRG in rats with L5 spinal nerve ligation. Pain 99 (2002) 111-120
13. Gavva N.R., Tamir R., Qu Y., Klionsky L., Zhang T.J., Immke D., Wang J., Zhu D., Vanderah T.W., Porreca F., Doherty E.M., Norman M.H., Wild K.D., Bannon A.W., Louis J.C., and Treanor J.J. AMG 9810 [(E)-3-(4-t-butylphenyl)-N-(2,3-dihydrobenzo[b][1,4] dioxin-6-yl)acrylamide], a novel vanilloid receptor 1 (TRPV1) antagonist with antihyperalgesic properties. J Pharmacol Exp Ther 313 (2005) 474-484
14. Ghilardi J.R., Rohrich H., Lindsay T.H., Sevcik M.A., Schwei M.J., Kubota K., Halvorson K.G., Poblete J., Chaplan S.R., Dubin A.E., Carruthers N.I., Swanson D., Kuskowski M., Flores C.M., Julius D., and Mantyh P.W. Selective blockade of the capsaicin receptor TRPV1 attenuates bone cancer pain. J Neurosci 25 (2005) 3126-3131
15. Hargreaves K., Dubner R., Brown F., Flores C., and Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32 (1988) 77-88
16. Honore P., Luger N.M., Sabino M.A., Schwei M.J., Rogers S.D., Mach D.B., O'Keefe P.F., Ramnaraine M.L., Clohisy D.R., and Mantyh P.W. Osteoprotegerin blocks bone cancer-induced skeletal destruction, skeletal pain and pain-related neurochemical reorganization of the spinal cord. Nat Med 6 (2000) 521-528
17. Honore P., Rogers S.D., Schwei M.J., Salak-Johnson J.L., Luger N.M., Sabino M.C., Clohisy D.R., and Mantyh P.W. Murine models of inflammatory, neuropathic and cancer pain each generates a unique set of neurochemical changes in the spinal cord and sensory neurons. Neuroscience 98 (2000) 585-598
18. Honore P., Wismer C.T., Mikusa J., Zhu C.Z., Zhong C., Gauvin D.M., Gomtsyan A., El Kouhen R., Lee C.H., Marsh K., Sullivan J.P., Faltynek C.R., and Jarvis M.F. A-425619 [1-isoquinolin-5-yl-3-(4-trifluoromethyl-benzyl)-urea], a novel transient receptor potential type V1 receptor antagonist, relieves pathophysiological pain associated with inflammation and tissue injury in rats. J Pharmacol Exp Ther 314 (2005) 410-421
19. Hudson L.J., Bevan S., Wotherspoon G., Gentry C., Fox A., and Winter J. VR1 protein expression increases in undamaged DRG neurons after partial nerve injury. Eur J Neurosci 13 (2001) 2105-2114
20. Ji R.R., Samad T.A., Jin S.X., Schmoll R., and Woolf C.J. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36 (2002) 57-68
21. Koizumi W., Toma H., Watanabe K., Katayama K., Kawahara M., Matsui K., Takiuchi H., Yoshino K., Araki N., Kodama K., Kimura H., Kono I., Hasegawa H., Hatanaka K., Hiraga K., and Takeda F. Efficacy and tolerability of cancer pain management with controlled-release oxycodone tablets in opioid-naive cancer pain patients, starting with 5 mg tablets. Jpn J Clin Oncol 34 (2004) 608-614
22. LaMotte R.H., Shain C.N., Simone D.A., and Tsai E.F. Neurogenic hyperalgesia: Psychophysical studies of underlying mechanisms. J Neurophysiol 66 (1991) 190-211
23. Lawson S.N. Phenotype and function of somatic primary afferent nociceptive neurones with C-, Adelta- or Aalpha/beta-fibres. Exp Physiol 87 (2002) 239-244
24. Lewinter R.D., Skinner K., Julius D., and Basbaum A.I. Immunoreactive TRPV-2 (VRL-1), a capsaicin receptor homolog, in the spinal cord of the rat. J Comp Neurol 470 (2004) 400-408
25. Liedtke W., and Friedman J.M. Abnormal osmotic regulation in trpv4-/- mice. Proc Natl Acad Sci U S A 100 (2003) 13698-13703
26. Luger N.M., Honore P., Sabino M.A., Schwei M.J., Rogers S.D., Mach D.B., Clohisy D.R., and Mantyh P.W. Osteoprotegerin diminishes advanced bone cancer pain. Cancer Res 61 (2001) 4038-4047
27. Luger N.M., Mach D.B., Sevcik M.A., and Mantyh P.W. Bone cancer pain: from model to mechanism to therapy. J Pain Symptom Manage 29 (2005) S32-S46
28. Ma Q.P. Vanilloid receptor homologue, VRL1, is expressed by both A- and C-fiber sensory neurons. Neuroreport 12 (2001) 3693-3695
29. Ma W., Zhang Y., Bantel C., and Eisenach J.C. Medium and large injured dorsal root ganglion cells increase TRPV-1, accompanied by increased alpha2C-adrenoceptor co-expression and functional inhibition by clonidine. Pain 113 (2005) 386-394
30. Mantyh P.W. Cancer pain and its impact on diagnosis, survival and quality of life. Nat Rev Neurosci 7 (2006) 797-809
31. McGaraughty S., Chu K.L., Faltynek C.R., and Jarvis M.F. Systemic and site-specific effects of A-425619, a selective TRPV1 receptor antagonist, on wide dynamic range neurons in CFA-treated and uninjured rats. J Neurophysiol 95 (2006) 18-25
32. Menendez L., Juarez L., Garcia E., Garcia-Suarez O., Hidalgo A., and Baamonde A. Analgesic effects of capsazepine and resiniferatoxin on bone cancer pain in mice. Neurosci Lett 393 (2006) 70-73
33. Menendez L., Lastra A., Fresno M.F., Llames S., Meana A., Hidalgo A., and Baamonde A. Initial thermal heat hypoalgesia and delayed hyperalgesia in a murine model of bone cancer pain. Brain Res 969 (2003) 102-109
34. Mercadante S., and Arcuri E. Breakthrough pain in cancer patients: Pathophysiology and treatment. Cancer Treat Rev 24 (1998) 425-432
35. Nagamine K., Ozaki N., Shinoda M., Asai H., Nishiguchi H., Mitsudo K., Tohnai I., Ueda M., and Sugiura Y. Mechanical allodynia and thermal hyperalgesia induced by experimental squamous cell carcinoma of the lower gingiva in rats. J Pain 7 (2006) 659-670
36. Nicholas R.S., Winter J., Wren P., Bergmann R., and Woolf C.J. Peripheral inflammation increases the capsaicin sensitivity of dorsal root ganglion neurons in a nerve growth factor-dependent manner. Neuroscience 91 (1999) 1425-1433
37. Pomonis J.D., Harrison J.E., Mark L., Bristol D.R., Valenzano K.J., and Walker K. N-(4-Tertiarybutylphenyl)-4-(3-cholorphyridin-2-yl)tetrahydropyrazine-1(2H)-carbox-amide (BCTC), a novel, orally effective vanilloid receptor 1 antagonist with analgesic properties, II: In vivo characterization in rat models of inflammatory and neuropathic pain. J Pharmacol Exp Ther 306 (2003) 387-393
38. Portenoy R.K. Cancer pain management. Clin Adv Hematol Oncol 3 (2005) 30-32
39. Portenoy R.K., and Lesage P. Management of cancer pain. Lancet 353 (1999) 1695-1700
40. Sakurada T., Matsumura T., Moriyama T., Sakurada C., Ueno S., and Sakurada S. Differential effects of intraplantar capsazepine and ruthenium red on capsaicin-induced desensitization in mice. Pharmacol Biochem Behav 75 (2003) 115-121
41. Sasamura T., Nakamura S., Iida Y., Fujii H., Murata J., Saiki I., Nojima H., and Kuraishi Y. Morphine analgesia suppresses tumor growth and metastasis in a mouse model of cancer pain produced by orthotopic tumor inoculation. Eur J Pharmacol 441 (2002) 185-191
42. Schwei M.J., Honore P., Rogers S.D., Salak-Johnson J.L., Finke M.P., Ramnaraine M.L., Clohisy D.R., and Mantyh P.W. Neurochemical and cellular reorganization of the spinal cord in a murine model of bone cancer pain. J Neurosci 19 (1999) 10886-10897
43. Shimosato G., Amaya F., Ueda M., Tanaka Y., Decosterd I., and Tanaka M. Peripheral inflammation induces up-regulation of TRPV2 expression in rat DRG. Pain 119 (2005) 225-232
44. Shimoyama M., Tanaka K., Hasue F., and Shimoyama N. A mouse model of neuropathic cancer pain. Pain 99 (2002) 167-174
45. Simone D.A., Nolano M., Johnson T., Wendelschafer-Crabb G., and Kennedy W.R. Intradermal injection of capsaicin in humans produces degeneration and subsequent reinnervation of epidermal nerve fibers: Correlation with sensory function. J Neurosci 18 (1998) 8947-8959
46. Simone D.A., Sorkin L.S., Oh U., Chung J.M., Owens C., LaMotte R.H., and Willis W.D. Neurogenic hyperalgesia: Central neural correlates in responses of spinothalamic tract neurons. J Neurophysiol 66 (1991) 228-246
47. Suzuki M., Mizuno A., Kodaira K., and Imai M. Impaired pressure sensation in mice lacking TRPV4. J Biol Chem 278 (2003) 22664-22668
48. Tohda C., Sasaki M., Konemura T., Sasamura T., Itoh M., and Kuraishi Y. Axonal transport of VR1 capsaicin receptor mRNA in primary afferents and its participation in inflammation-induced increase in capsaicin sensitivity. J Neurochem 76 (2001) 1628-1635
49. Tominaga M., and Caterina M.J. Thermosensation and pain. J Neurobiol 61 (2004) 3-12
50. Tominaga M., and Tominaga T. Structure and function of TRPV1. Pflugers Arch 451 (2005) 143-150
51. Torebjork H.E., Lundberg L.E., and LaMotte R.H. Central changes in processing of mechanoreceptive input in capsaicin-induced secondary hyperalgesia in humans. J Physiol 448 (1992) 765-780
52. Valtschanoff J.G., Rustioni A., Guo A., and Hwang S.J. Vanilloid receptor VR1 is both presynaptic and postsynaptic in the superficial laminae of the rat dorsal horn. J Comp Neurol 436 (2001) 225-235
53. Wacnik P.W., Eikmeier L.J., Ruggles T.R., Ramnaraine M.L., Walcheck B.K., Beitz A.J., and Wilcox G.L. Functional interactions between tumor and peripheral nerve: Morphology, algogen identification, and behavioral characterization of a new murine model of cancer pain. J Neurosci 21 (2001) 9355-9366
54. Walker K.M., Urban L., Medhurst S.J., Patel S., Panesar M., Fox A.J., and McIntyre P. The VR1 antagonist capsazepine reverses mechanical hyperalgesia in models of inflammatory and neuropathic pain. J Pharmacol Exp Ther 304 (2003) 56-62
55. Winston J., Toma H., Shenoy M., and Pasricha P.J. Nerve growth factor regulates VR-1 mRNA levels in cultures of adult dorsal root ganglion neurons. Pain 89 (2001) 181-186
56. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16 (1983) 109-110