Novel TRPM8 antagonist attenuates cold hypersensitivity after peripheral nerve injury in rats

Journal of Pharmacology and Experimental Therapeutics

Volumn 349, Issue 4, 2014, Pages 47-55

  Patel, Ryan ^a   Gonçalves, Leonor ^a   Newman, Robert ^b   Jiang, Feng Li ^c   Goldby, Anne ^b   Reeve, Jennifer ^b   Hendrick, Alan ^b   Teall, Martin ^b   Hannah, Duncan ^b   Almond, Sarah ^b   Brice, Nicola ^b   Dickenson, Anthony H ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b Takeda Cambridge Ltd   (United Kingdom)

^c Takeda Singapore (S) Pte Ltd   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; BEHAVIOR, ANIMAL; CALCIUM; CRYOPYRIN-ASSOCIATED PERIODIC SYNDROMES; DISEASE MODELS, ANIMAL; ELECTROPHYSIOLOGICAL PHENOMENA; HEK293 CELLS; HUMANS; MALE; NICOTINIC ACIDS; PERIPHERAL NERVE INJURIES; RATS; RATS, SPRAGUE-DAWLEY; TRPM CATION CHANNELS;

EID: 84896448849     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.113.211243     Document Type: Article

References (55)

1. Almeida MC, Hew-Butler T, Soriano RN, Rao S, Wang W, Wang J, Tamayo N, Oliveira DL, Nucci TB, and Aryal P, et al. (2012) Pharmacological blockade of the cold receptor TRPM8 attenuates autonomic and behavioral cold defenses and decreases deep body temperature. J Neurosci 32:2086-2099.
2. Bautista DM, Jordt S-E, Nikai T, Tsuruda PR, Read AJ, Poblete J, Yamoah EN, Basbaum AI, and Julius D (2006) TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124:1269-1282.
3. Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI, Stucky CL, Jordt S-E, and Julius D (2007) The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448:204-208.
4. Brignell JL, Chapman V, and Kendall DA (2008) Comparison of icilin- and coldevoked responses of spinal neurones, and their modulation of mechanical activity, in a model of neuropathic pain. Brain Res 1215:87-96.
5. Calvo RR, Meegalla SK, Parks DJ, Parsons WH, Ballentine SK, Lubin ML, Schneider C, Colburn RW, Flores CM, and Player MR (2012) Discovery of vinylcycloalkyl-substituted benzimidazole TRPM8 antagonists effective in the treatment of cold allodynia. Bioorg Med Chem Lett 22:1903-1907.
6. Chaplan SR, Bach FW, Pogrel JW, Chung JM, and Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55-63.
7. Colburn RW, Lubin ML, Stone DJ, Jr, Wang Y, Lawrence D, D'Andrea MR, Brandt MR, Liu Y, Flores CM, and Qin N (2007) Attenuated cold sensitivity in TRPM8 null mice. Neuron 54:379-386.
8. Descoeur J, Pereira V, Pizzoccaro A, Francois A, Ling B, Maffre V, Couette B, Busserolles J, Courteix C, and Noel J, et al. (2011) Oxaliplatin-induced cold hypersensitivity is due to remodelling of ion channel expression in nociceptors. EMBO Mol Med 3:266-278.
9. Dhaka A, Murray AN, Mathur J, Earley TJ, Petrus MJ, and Patapoutian A (2007) TRPM8 is required for cold sensation in mice. Neuron 54:371-378.
10. Ding Z, Gomez T, Werkheiser JL, Cowan A, and Rawls SM (2008) Icilin induces a hyperthermia in rats that is dependent on nitric oxide production and NMDA receptor activation. Eur J Pharmacol 578:201-208.
11. Gavva NR, Davis C, Lehto SG, Rao S, Wang W, and Zhu DX (2012) Transient receptor potential melastatin 8 (TRPM8) channels are involved in body temperature regulation. Mol Pain 8:36.
12. Kim SH and Chung JM (1992) An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50:355-363.
13. Jørum E, Warncke T, and Stubhaug A (2003) Cold allodynia and hyperalgesia in neuropathic pain: the effect of N-methyl-D-aspartate (NMDA) receptor antagonist ketamine - a double-blind, cross-over comparison with alfentanil and placebo. Pain 101:229-235.
14. Kaley TJ and Deangelis LM (2009) Therapy of chemotherapy-induced peripheral neuropathy. Br J Haematol 145:3-14.
15. Karashima Y, Talavera K, Everaerts W, Janssens A, Kwan KY, Vennekens R, Nilius B, and Voets T (2009) TRPA1 acts as a cold sensor in vitro and in vivo. Proc Natl Acad Sci USA 106:1273-1278.
16. Katsura H, Obata K, Mizushima T, Yamanaka H, Kobayashi K, Dai Y, Fukuoka T, Tokunaga A, Sakagami M, and Noguchi K (2006) Antisense knock down of TRPA1, but not TRPM8, alleviates cold hyperalgesia after spinal nerve ligation in rats. Exp Neurol 200:112-123.
17. Knowlton WM, Bifolck-Fisher A, Bautista DM, and McKemy DD (2010) TRPM8, but not TRPA1, is required for neural and behavioral responses to acute noxious cold temperatures and cold-mimetics in vivo. Pain 150:340-350.
18. Knowlton WM, Daniels RL, Palkar R, McCoy DD, and McKemy DD (2011) Pharmacological blockade of TRPM8 ion channels alters cold and cold pain responses in mice. PLoS ONE 6:e25894.
19. Knowlton WM, Palkar R, Lippoldt EK, McCoy DD, Baluch F, Chen J, and McKemy DD (2013) A sensory-labeled line for cold: TRPM8-expressing sensory neurons define the cellular basis for cold, cold pain, and cooling-mediated analgesia. J Neurosci 33:2837-2848.
20. Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang D-S, Woolf CJ, and Corey DP (2006) TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50:277-289.
21. Lashinger ES, Steiginga MS, Hieble JP, Leon LA, Gardner SD, Nagilla R, Davenport EA, Hoffman BE, Laping NJ, and Su X (2008) AMTB, a TRPM8 channel blocker: evidence in rats for activity in overactive bladder and painful bladder syndrome. Am J Physiol Renal Physiol 295:F803-F810.
22. Leith JL, Koutsikou S, Lumb BM, and Apps R (2010) Spinal processing of noxious and innocuous cold information: differential modulation by the periaqueductal gray. J Neurosci 30:4933-4942.
23. Lippoldt EK, Elmes RR, McCoy DD, Knowlton WM, and McKemy DD (2013) Artemin, a glial cell line-derived neurotrophic factor family member, induces TRPM8-dependent cold pain. J Neurosci 33:12543-12552.
24. Madrid R, de la Peña E, Donovan-Rodriguez T, Belmonte C, and Viana F (2009) Variable threshold of trigeminal cold-thermosensitive neurons is determined by a balance between TRPM8 and Kv1 potassium channels. J Neurosci 29:3120-3131.
25. Madrid R, Donovan-Rodríguez T, Meseguer V, Acosta MC, Belmonte C, and Viana F (2006) Contribution of TRPM8 channels to cold transduction in primary sensory neurons and peripheral nerve terminals. J Neurosci 26:12512-12525.
26. Maier C, Baron R, Tölle TR, Binder A, Birbaumer N, Birklein F, Gierthmühlen J, Flor H, Geber C, and Huge V, et al. (2010) Quantitative sensory testing in the German Research Network on Neuropathic Pain (DFNS): somatosensory abnormalities in 1236 patients with different neuropathic pain syndromes. Pain 150: 439-450.
27. Masamoto Y, Kawabata F, and Fushiki T (2009) Intragastric administration of TRPV1, TRPV3, TRPM8, and TRPA1 agonists modulates autonomic thermoregulation in different manners in mice. Biosci Biotechnol Biochem 73:1021-1027.
28. McCoy ES, Taylor-Blake B, Street SE, Pribisko AL, Zheng J, and Zylka MJ (2013) Peptidergic CGRPa primary sensory neurons encode heat and itch and tonically suppress sensitivity to cold. Neuron 78:138-151.
29. McKemy DD (2013) The molecular and cellular basis of cold sensation. ACS Chem Neurosci 4:238-247.
30. McKemy DD, Neuhausser WM, and Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52-58.
31. Minett MS, Nassar MA, Clark AK, Passmore G, Dickenson AH, Wang F, Malcangio M, and Wood JN (2012) Distinct Nav1.7-dependent pain sensations require different sets of sensory and sympathetic neurons. Nat Commun 3:791.
32. Munns C, AlQatari M, and Koltzenburg M (2007) Many cold sensitive peripheral neurons of the mouse do not express TRPM8 or TRPA1. Cell Calcium 41:331-342.
33. Ochoa JL and Yarnitsky D (1994) The triple cold syndrome. Cold hyperalgesia, cold hypoaesthesia and cold skin in peripheral nerve disease. Brain 117:185-197.
34. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, Earley TJ, Dragoni I, McIntyre P, and Bevan S, et al. (2002) A TRP channel that senses cold stimuli and menthol. Cell 108:705-715.
35. Pertusa M, Madrid R, Morenilla-Palao C, Belmonte C, and Viana F (2012) N-Glycosylation of TRPM8 ion channels modulates temperature sensitivity of cold thermoreceptor neurons. J Biol Chem 287:18218-18229.
36. Quick K, Zhao J, Eijkelkamp N, Linley JE, Rugiero F, Cox JJ, Raouf R, Gringhuis M, Sexton JE, and Abramowitz J (2012) TRPC3 and TRPC6 are essential for normal mechanotransduction in subsets of sensory neurons and cochlear hair cells. Open Biol 2: 120068.
37. Rahman W, Suzuki R, Webber M, Hunt SP, and Dickenson AH (2006) Depletion of endogenous spinal 5-HT attenuates the behavioural hypersensitivity to mechanical and cooling stimuli induced by spinal nerve ligation. Pain 123:264-274.
38. 2 regulates the activation and desensitization of TRPM8 channels through the TRP domain. Nat Neurosci 8:626-634.
39. Serra J, Solà R, Quiles C, Casanova-Molla J, Pascual V, Bostock H, and Valls-Solé J (2009) C-nociceptors sensitized to cold in a patient with small-fiber neuropathy and cold allodynia. Pain 147:46-53.
40. Sikandar S, Ronga I, Iannetti GD, and Dickenson AH (2013) Neural coding of nociceptive stimuli-from rat spinal neurones to human perception. Pain 154: 1263-1273.
41. Simone DA and Kajander KC (1996) Excitation of rat cutaneous nociceptors by noxious cold. Neurosci Lett 213:53-56.
42. Suzuki R, Kontinen VK, Matthews E, Williams E, and Dickenson AH (2000) Enlargement of the receptive field size to low intensity mechanical stimulation in the rat spinal nerve ligation model of neuropathy. Exp Neurol 163:408-413.
43. Suzuki R, Matthews EA, and Dickenson AH (2001) Comparison of the effects of MK-801, ketamine and memantine on responses of spinal dorsal horn neurones in a rat model of mononeuropathy. Pain 91:101-109.
44. Takashima Y, Daniels RL, Knowlton W, Teng J, Liman ER, and McKemy DD (2007) Diversity in the neural circuitry of cold sensing revealed by genetic axonal labeling of transient receptor potential melastatin 8 neurons. J Neurosci 27:14147-14157.
45. Taylor BK, Abhyankar SS, Vo N-TT, Kriedt CL, Churi SB, and Urban JH (2007) Neuropeptide Y acts at Y1 receptors in the rostral ventral medulla to inhibit neuropathic pain. Pain 131:83-95.
46. Urch C and Dickenson A (2003) In vivo single unit extracellular recordings from spinal cord neurones of rats. Brain Res Brain Res Protoc 12:26-34.
47. Viana F, de la Peña E, and Belmonte C (2002) Specificity of cold thermotransduction is determined by differential ionic channel expression. Nat Neurosci 5:254-260.
48. Wang H, Sun H, Della Penna K, Benz RJ, Xu J, Gerhold DL, Holder DJ, and Koblan KS (2002) Chronic neuropathic pain is accompanied by global changes in gene expression and shares pathobiology with neurodegenerative diseases. Neuroscience 114:529-546.
49. Wasner G, Naleschinski D, Binder A, Schattschneider J, McLachlan EM, and Baron R (2008) The effect of menthol on cold allodynia in patients with neuropathic pain. Pain Med 9:354-358.
50. Watson C, Paxinos G, Kayalioglu G, and Heise C (2009) Atlas of the Rat Spinal Cord, in The Spinal Cord, Chapter 15. Charles W, George P, and Gulgun K eds) pp 238-306, Academic Press, San Diego.
51. Woolf CJ and Thompson SW (1991) The induction and maintenance of central sensitization is dependent on N-methyl-D-aspartic acid receptor activation; implications for the treatment of post-injury pain hypersensitivity states. Pain 44: 293-299.
52. Yarnitsky D and Ochoa JL (1990) Release of cold-induced burning pain by block of cold-specific afferent input. Brain 113:893-902.
53. Zimmermann K, Leffler A, Babes A, Cendan CM, Carr RW, Kobayashi J-i, Nau C, Wood JN, and Reeh PW (2007) Sensory neuron sodium channel Nav1.8 is essential for pain at low temperatures. Nature 447:855-858.
54. Zimmermann K, Lennerz JK, Hein A, Link AS, Kaczmarek JS, Delling M, Uysal S, Pfeifer JD, Riccio A, and Clapham DE (2011) Transient receptor potential cation channel, subfamily C, member 5 (TRPC5) is a cold-transducer in the peripheral nervous system. Proc Natl Acad Sci USA 108:18114-18119.
55. Zimmermann M (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16:109-110.