AMG2850, a potent and selective TRPM8 antagonist, is not effective in rat models of inflammatory mechanical hypersensitivity and neuropathic tactile allodynia

Naunyn-Schmiedeberg's Archives of Pharmacology

Volumn 388, Issue 4, 2015, Pages 465-476

  Lehto, Sonya G ^a   Weyer, Andy D ^b   Zhang, Maosheng ^a   Youngblood, Beth D ^a   Wang, Judy ^a   Wang, Weiya ^a   Kerstein, Patrick C ^b   Davis, Carl ^a   Wild, Kenneth D ^a   Stucky, Cheryl L ^b   Gavva, Narender R ^a  

^a AMGEN INC   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

AMG2850; Hypersensitivity; Inflammatory; Neuropathic; Pain; Rat; Small molecule; Therapeutic; TRPM8

Indexed keywords

8 (4 (TRIFLUOROMETHYL)PHENYL) N ((S) 1,1,1 TRIFLUOROPROPAN 2 YL) 5,6 DIHYDRO 1,7 NAPHTHYRIDINE 7(8H) CARBOXAMIDE); ANALGESIC AGENT; GABAPENTIN; INDOMETACIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; TRANSIENT RECEPTOR POTENTIAL CHANNEL M8; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; VANILLOID RECEPTOR ANTAGONIST; AMG2850; CALCIUM; FREUND ADJUVANT; ICILIN; MENTHOL; NAPHTHYRIDINE DERIVATIVE; PYRIMIDINONE DERIVATIVE; TRANSIENT RECEPTOR POTENTIAL CHANNEL M; TRPM8 PROTEIN, RAT;

ACTION POTENTIAL; ADULT; ALLODYNIA; ANALGESIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN-TO-PLASMA RATIO; CHRONIC PAIN; COLD SENSITIVITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSE RESPONSE; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG EFFICACY; HYPERSENSITIVITY; IN VITRO STUDY; IN VIVO STUDY; MALE; MECHANICAL HYPERSENSITIVITY; NEUROPATHIC PAIN; NEUROPATHIC TACTILE ALLODYNIA; NONHUMAN; PLASMA CLEARANCE; RAT; THERAPY EFFECT; ANIMAL; ANIMAL BEHAVIOR; ANTAGONISTS AND INHIBITORS; BLOOD PRESSURE; BRAIN; C57BL MOUSE; CHO CELL LINE; COLD; CRICETULUS; DRUG EFFECTS; HAMSTER; HUMAN; HYPERALGESIA; INJURIES; METABOLISM; PAIN; SCIATIC NERVE; SPRAGUE DAWLEY RAT;

ACTION POTENTIALS; ANIMALS; BEHAVIOR, ANIMAL; BLOOD PRESSURE; BRAIN; CALCIUM; CHO CELLS; COLD TEMPERATURE; CRICETINAE; CRICETULUS; FREUND'S ADJUVANT; HUMANS; HYPERALGESIA; MALE; MENTHOL; MICE, INBRED C57BL; NAPHTHYRIDINES; PAIN; PYRIMIDINONES; RATS; RATS, SPRAGUE-DAWLEY; SCIATIC NERVE; TRPM CATION CHANNELS;

EID: 84925536714     PISSN: 00281298     EISSN: 14321912     Source Type: Journal    
DOI: 10.1007/s00210-015-1090-9     Document Type: Article

References (61)

1. Almaraz L, Manenschijn JA, de la Pena E, Viana F (2014) TRPM8. Handb Exp Pharmacol 222:547-579
2. Almeida MC, Hew-Butler T, Soriano RN, Rao S, Wang W, Wang J, Tamayo N, Oliveira DL, Nucci TB, Aryal P, Garami A, Bautista D, Gavva NR, Romanovsky AA (2012) Pharmacological blockade of the cold receptor TRPM8 attenuates autonomic and behavioral cold defenses and decreases deep body temperature. J Neurosci: Off J Soc Neurosci 32:2086-2099
3. Anttila V, Winsvold BS, Gormley P, Kurth T, Bettella F, McMahon G, Kallela M, Malik R, de Vries B, Terwindt G, Medland SE, Todt U, McArdle WL, Quaye L, Koiranen M, Ikram MA, Lehtimaki T, Stam AH, Ligthart L, Wedenoja J, Dunham I, Neale BM, Palta P, Hamalainen E, Schurks M, Rose LM, Buring JE, Ridker PM, Steinberg S, Stefansson H, Jakobsson F, Lawlor DA, Evans DM, Ring SM, Farkkila M, Artto V, Kaunisto MA, Freilinger T, Schoenen J, Frants RR, Pelzer N, Weller CM, Zielman R, Heath AC, Madden PA, Montgomery GW, Martin NG, Borck G, Gobel H, Heinze A, Heinze-Kuhn K, Williams FM, Hartikainen AL, Pouta A, van den Ende J, Uitterlinden AG, Hofman A, Amin N, Hottenga JJ, Vink JM, Heikkila K, Alexander M, Muller-Myhsok B, Schreiber S, Meitinger T, Wichmann HE, Aromaa A, Eriksson JG, Traynor BJ, Trabzuni D, Rossin E, Lage K, Jacobs SB, Gibbs JR, Birney E, Kaprio J, Penninx BW, Boomsma DI, van Duijn C, Raitakari O, Jarvelin MR, Zwart JA, Cherkas L, Strachan DP, Kubisch C, Ferrari MD, van den Maagdenberg AM, Dichgans M, Wessman M, Smith GD, Stefansson K, Daly MJ, Nyholt DR, Chasman DI, Palotie A (2013) Genome-wide meta-analysis identifies new susceptibility loci for migraine. Nat Genet 45:912-917
4. Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI, Stucky CL, Jordt SE, Julius D (2007) The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448:204-208
5. Belmonte C, Brock JA, Viana F (2009) Converting cold into pain. Exp Brain Res Exp Hirnforschung Exp Cerebrale 196:13-30
6. Brignell JL, Chapman V, Kendall DA (2008) Comparison of icilin- and cold-evoked responses of spinal neurones, and their modulation of mechanical activity, in a model of neuropathic pain. Brain Res 1215:87-96
7. 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
8. Chasman DI, Schurks M, Anttila V, de Vries B, Schminke U, Launer LJ, Terwindt GM, van den Maagdenberg AM, Fendrich K, Volzke H, Ernst F, Griffiths LR, Buring JE, Kallela M, Freilinger T, Kubisch C, Ridker PM, Palotie A, Ferrari MD, Hoffmann W, Zee RY, Kurth T (2011) Genome-wide association study reveals three susceptibility loci for common migraine in the general population. Nat Genet 43:695-698
9. Chasman DI, Anttila V, Buring JE, Ridker PM, Schurks M, Kurth T (2014) Selectivity in genetic association with sub-classified migraine in women. PLoS Genet 10:e1004366
10. Colburn RW, Lubin ML, Stone DJ Jr, Wang Y, Lawrence D, D'Andrea MR, Brandt MR, Liu Y, Flores CM, Qin N (2007) Attenuated cold sensitivity in TRPM8 null mice. Neuron 54:379-386
11. Daniels RL, McKemy DD (2007) Mice left out in the cold: commentary on the phenotype of TRPM8-nulls. Mol Pain 3:23
12. Descoeur J, Pereira V, Pizzoccaro A, Francois A, Ling B, Maffre V, Couette B, Busserolles J, Courteix C, Noel J, Lazdunski M, Eschalier A, Authier N, Bourinet E (2011) Oxaliplatin-induced cold hypersensitivity is due to remodelling of ion channel expression in nociceptors. EMBO Mol Med 3:266-278
13. Dhaka A, Viswanath V, Patapoutian A (2006) Trp ion channels and temperature sensation. Annu Rev Neurosci 29:135-161
14. Dhaka A, Murray AN, Mathur J, Earley TJ, Petrus MJ, Patapoutian A (2007) TRPM8 is required for cold sensation in mice. Neuron 54:371-378
15. Dhaka A, Earley TJ, Watson J, Patapoutian A (2008) Visualizing cold spots: TRPM8-expressing sensory neurons and their projections. J Neurosci: Off J Soc Neurosci 28:566-575
16. Dixon WJ (1980) Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 20:441-462
17. Esserlind AL, Christensen AF, Le H, Kirchmann M, Hauge AW, Toyserkani NM, Hansen T, Grarup N, Werge T, Steinberg S, Bettella F, Stefansson H, Olesen J (2013) Replication and meta-analysis of common variants identifies a genome-wide significant locus in migraine. Eur J Neurol: Off J Eur Fed Neurol Soc 20:765-772
18. Ferrer-Montiel A, Fernandez-Carvajal A, Planells-Cases R, Fernandez-Ballester G, Gonzalez-Ros JM, Messeguer A, Gonzalez-Muniz R (2012) Advances in modulating thermosensory TRP channels. Exp Opin Ther Patents 22:999-1017
19. Fleetwood-Walker SM, Proudfoot CW, Garry EM, Allchorne A, Vinuela-Fernandez I, Mitchell R (2007) Cold comfort pharm. Trends Pharmacol Sci 28:621-628
20. Freilinger T, Anttila V, de Vries B, Malik R, Kallela M, Terwindt GM, Pozo-Rosich P, Winsvold B, Nyholt DR, van Oosterhout WP, Artto V, Todt U, Hamalainen E, Fernandez-Morales J, Louter MA, Kaunisto MA, Schoenen J, Raitakari O, Lehtimaki T, Vila-Pueyo M, Gobel H, Wichmann E, Sintas C, Uitterlinden AG, Hofman A, Rivadeneira F, Heinze A, Tronvik E, van Duijn CM, Kaprio J, Cormand B, Wessman M, Frants RR, Meitinger T, Muller-Myhsok B, Zwart JA, Farkkila M, Macaya A, Ferrari MD, Kubisch C, Palotie A, Dichgans M, van den Maagdenberg AM (2012) Genome-wide association analysis identifies susceptibility loci for migraine without aura. Nat Genet 44:777-782
21. Gauchan P, Andoh T, Kato A, Kuraishi Y (2009) Involvement of increased expression of transient receptor potential melastatin 8 in oxaliplatin-induced cold allodynia in mice. Neurosci Lett 458:93-95
22. Gavva NR, Bannon AW, Hovland DN Jr, Lehto SG, Klionsky L, Surapaneni S, Immke DC, Henley C, Arik L, Bak A, Davis J, Ernst N, Hever G, Kuang R, Shi L, Tamir R, Wang J, Wang W, Zajic G, Zhu D, Norman MH, Louis JC, Magal E, Treanor JJ (2007) Repeated administration of vanilloid receptor TRPV1 antagonists attenuates hyperthermia elicited by TRPV1 blockade. J Pharmacol Exp Ther 323:128-137
23. Gavva NR, Davis C, Lehto SG, Rao S, Wang W, Zhu DX (2012) Transient receptor potential melastatin 8 (TRPM8) channels are involved in body temperature regulation. Mol Pain 8:36
24. Harrington AM, Hughes PA, Martin CM, Yang J, Castro J, Isaacs NJ, Blackshaw LA, Brierley SM (2011) A novel role for TRPM8 in visceral afferent function. Pain 152:1459-1468
25. Horne DB, Tamayo NA, Bartberger MD, Bo Y, Clarine J, Davis CD, Gore VK, Kaller MR, Lehto SG, Ma VV, Nishimura N, Nguyen TT, Tang P, Wang W, Youngblood BD, Zhang M, Gavva NR, Monenschein H and Norman MH (2014) Optimization of potency and pharmacokinetic properties of tetrahydroisoquinoline transient receptor potential melastatin 8 (TRPM8) Antagonists. J Med Chem
26. Kim SH, Chung JM (1992) An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50:355-363
27. Klein AH, Sawyer CM, Carstens MI, Tsagareli MG, Tsiklauri N, Carstens E (2010) Topical application of L-menthol induces heat analgesia, mechanical allodynia, and a biphasic effect on cold sensitivity in rats. Behav Brain Res 212:179-186
28. Klionsky L, Tamir R, Gao B, Wang W, Immke DC, Nishimura N, Gavva NR (2007) Species-specific pharmacology of trichloro(sulfanyl)ethyl benzamides as transient receptor potential ankyrin 1 (TRPA1) antagonists. Mol Pain 3:39
29. Knowlton WM, McKemy DD (2011) TRPM8: from cold to cancer, peppermint to pain. Curr Pharm Biotechnol 12:68-77
30. Knowlton WM, Bifolck-Fisher A, Bautista DM, 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
31. Knowlton WM, Daniels RL, Palkar R, McCoy DD, McKemy DD (2011) Pharmacological blockade of TRPM8 ion channels alters cold and cold pain responses in mice. PLoS One 6:e25894
32. Knowlton WM, Palkar R, Lippoldt EK, McCoy DD, Baluch F, Chen J, 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: Off J Soc Neurosci 33:2837-2848
33. Koltzenburg M, Stucky CL, Lewin GR (1997) Receptive properties of mouse sensory neurons innervating hairy skin. J Neurophysiol 78:1841-1850
34. Kwan KY, Glazer JM, Corey DP, Rice FL, Stucky CL (2009) TRPA1 modulates mechanotransduction in cutaneous sensory neurons. J Neurosci 29:4808-4819
35. Le Poul E, Hisada S, Mizuguchi Y, Dupriez VJ, Burgeon E, Detheux M (2002) Adaptation of aequorin functional assay to high throughput screening. J Biomol Screen 7:57-65
36. Liu Y, Qin N (2011) TRPM8 in health and disease: cold sensing and beyond. Adv Exp Med Biol 704:185-208
37. Liu B, Fan L, Balakrishna S, Sui A, Morris JB, Jordt SE (2013) TRPM8 is the principal mediator of menthol-induced analgesia of acute and inflammatory pain. Pain 154:2169-2177
38. Malkia A, Pertusa M, Fernandez-Ballester G, Ferrer-Montiel A, Viana F (2009) Differential role of the menthol-binding residue Y745 in the antagonism of thermally gated TRPM8 channels. Mol Pain 5:62
39. Malkia A, Morenilla-Palao C, Viana F (2011) The emerging pharmacology of TRPM8 channels: hidden therapeutic potential underneath a cold surface. Curr Pharm Biotechnol 12:54-67
40. McCoy DD, Knowlton WM, McKemy DD (2011) Scraping through the ice: uncovering the role of TRPM8 in cold transduction. Am J Physiol Regul, Integrative Comp Physiol 300:R1278-1287
41. McKemy DD, Neuhausser WM, Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52-58
42. National Research Council Committee for the Update of the Guide for the C and Use of Laboratory A (2011) The National Academies Collection: reports funded by National Institutes of Health, in guide for the care and use of laboratory animals. National Academies Press (US) National Academy of Sciences, Washington
43. Nieto-Posadas A, Jara-Oseguera A, Rosenbaum T (2011) TRP channel gating physiology. Curr Top Med Chem 11:2131-2150
44. Park CK, Kim MS, Fang Z, Li HY, Jung SJ, Choi SY, Lee SJ, Park K, Kim JS, Oh SB (2006) Functional expression of thermo-transient receptor potential channels in dental primary afferent neurons: implication for tooth pain. J Biol Chem 281:17304-17311
45. Parks DJ, Parsons WH, Colburn RW, Meegalla SK, Ballentine SK, Illig CR, Qin N, Liu Y, Hutchinson TL, Lubin ML, Stone DJ Jr, Baker JF, Schneider CR, Ma J, Damiano BP, Flores CM, Player MR (2011) Design and optimization of benzimidazole-containing transient receptor potential melastatin 8 (TRPM8) antagonists. J Med Chem 54:233-247
46. Patel R, Goncalves L, Newman R, Jiang FL, Goldby A, Reeve J, Hendrick A, Teall M, Hannah D, Almond S, Brice N, Dickenson AH (2014) Novel TRPM8 antagonist attenuates cold hypersensitivity after peripheral nerve injury in rats. J Pharmacol Exp Ther 349:47-55
47. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, Earley TJ, Dragoni I, McIntyre P, Bevan S, Patapoutian A (2002) A TRP channel that senses cold stimuli and menthol. Cell 108:705-715
48. Proudfoot CJ, Garry EM, Cottrell DF, Rosie R, Anderson H, Robertson DC, Fleetwood-Walker SM, Mitchell R (2006) Analgesia mediated by the TRPM8 cold receptor in chronic neuropathic pain. Current Biol: CB 16:1591-1605
49. Reid G, Flonta ML (2001) Physiology. Cold current in thermoreceptive neurons. Nature 413:480
50. Schurks M (2011) Genetics of migraine in the age of genome-wide association studies. J Headache Pain
51. Stucky CL, Koltzenburg M, Schneider M, Engle MG, Albers KM, Davis BM (1999) Overexpression of nerve growth factor in skin selectively affects the survival and functional properties of nociceptors. J Neurosci 19:8509-8516
52. Stucky CL, Dubin AE, Jeske NA, Malin SA, McKemy DD, Story GM (2009) Roles of transient receptor potential channels in pain. Brain Res Rev 60:2-23
53. Su L, Wang C, Yu Y-h, Ren Y-y, Xie K-l, Wang G-l (2011) Role of TRPM8 in dorsal root ganglion in nerve injury-induced chronic pain. BMC Neurosci 12:120
54. Tajino K, Matsumura K, Kosada K, Shibakusa T, Inoue K, Fushiki T, Hosokawa H, Kobayashi S (2007) Application of menthol to the skin of whole trunk in mice induces autonomic and behavioral heat-gain responses. Am J Physiol Regul, Integrative Comp Physiol 293:R2128-2135
55. Tajino K, Hosokawa H, Maegawa S, Matsumura K, Dhaka A, Kobayashi S (2011) Cooling-sensitive TRPM8 is thermostat of skin temperature against cooling. PLoS One 6:e17504
56. Takashima Y, Daniels RL, Knowlton W, Teng J, Liman ER, 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: Off J Soc Neurosci 27:14147-14157
57. Tamayo NA, Bo Y, Gore V, Ma V, Nishimura N, Tang P, Deng H, Klionsky L, Lehto SG, Wang W, Youngblood B, Chen J, Correll TL, Bartberger MD, Gavva NR, Norman MH (2012) Fused piperidines as a novel class of potent and orally available transient receptor potential melastatin type 8 (TRPM8) antagonists. J Med Chem 55:1593-1611
58. Werkheiser JL, Rawls SM, Cowan A (2006) Mu and kappa opioid receptor agonists antagonize icilin-induced wet-dog shaking in rats. Eur J Pharmacol 547:101-105
59. Xing H, Chen M, Ling J, Tan W, Gu JG (2007) TRPM8 mechanism of cold allodynia after chronic nerve injury. J Neurosci: Off J Soc Neurosci 27:13680-13690
60. Youngblood B, Hever G, Zhang M, Sun H, Willee A, Rubino J, Zhu D, Deng H, Wang T, Magal E, Lee D, Manning B, Wild K, Lehto SG (2008) Validation of a novel, automated assay of inflammation-induced allodynia in rats. Soc Neurosci Abstracts 468:13
61. Zimmermann K, Lennerz JK, Hein A, Link AS, Kaczmarek JS, Delling M, Uysal S, Pfeifer JD, Riccio A, 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 U S A 108:18114-18119