Anti-calmodulins and tricyclic adjuvants in pain therapy block the TRPV1 channel

PLoS ONE

Volumn 2, Issue 6, 2007, Pages

  Oláh, Zoltán ^a,b,c   Jósvay, Katalin ^a   Pecze, László ^a   Letoha, Tamás ^b,d   Babai, Norbert ^e   Budai, Dénes ^d   Ötvös, Ferenc ^a   Szalma, Sándor ^c   Vizler, Csaba ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b Acheuron Hungary Ltd   (Hungary)

^c MeTa Informatics and Acheuron Pharmaceuticals Inc   (United States)

^d UNIVERSITY OF SZEGED   (Hungary)

^e UNIVERSITY OF PÉCS   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

AMITRIPTYLINE; CALCIUM CHANNEL; CALCIUM ION; CALMIDAZOLIUM; CALMODULIN; CALMODULIN INHIBITOR; CAPSAZEPINE; CHLORPROMAZINE; CLOTRIMAZOLE; FLUPHENAZINE; GABAPENTIN; MICONAZOLE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROLEPTIC AGENT; TRIFLUOPERAZINE; VANILLOID RECEPTOR 1; AGENTS ACTING ON THE PERIPHERAL NERVOUS AND NEUROMUSCULAR SYSTEMS; CALCIUM; CAPSAICIN; ENZYME INHIBITOR; IMIDAZOLE DERIVATIVE; TRICYCLIC ANTIDEPRESSANT AGENT; VANILLOID RECEPTOR;

ACIDITY; ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL STRAIN 3T3; CHANNEL GATING; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DRUG STRUCTURE; HUMAN; HUMAN CELL; IN VIVO STUDY; INHIBITION KINETICS; LAMINECTOMY; MICROIONTOPHORESIS; MOTONEURON; NERVE CELL; NOCICEPTION; NONHUMAN; PAIN; PROTEIN EXPRESSION; RAT; RECEPTOR BLOCKING; SENSORY GANGLION; STRUCTURE ACTIVITY RELATION; ADJUVANT CHEMOTHERAPY; ANIMAL; CELL CULTURE; CELL MEMBRANE POTENTIAL; CHEMICAL STRUCTURE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; FIBROBLAST; KERATINOCYTE; MALE; METABOLISM; MOUSE; WISTAR RAT;

RATTUS; RUMEX;

ANIMALS; ANTIDEPRESSIVE AGENTS, TRICYCLIC; ANTIPSYCHOTIC AGENTS; CALCIUM; CALMODULIN; CAPSAICIN; CELLS, CULTURED; CHEMOTHERAPY, ADJUVANT; CHLORPROMAZINE; ENZYME INHIBITORS; FIBROBLASTS; HUMANS; IMIDAZOLES; ION CHANNEL GATING; KERATINOCYTES; MALE; MEMBRANE POTENTIALS; MICE; MODELS, MOLECULAR; NEURONS; NIH 3T3 CELLS; PAIN; RATS; RATS, WISTAR; SENSORY SYSTEM AGENTS; TRPV CATION CHANNELS;

EID: 38849209195     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0000545     Document Type: Article

References (58)

1. Olah Z, Szabo T, Karai L, Hough C, Field's RD, et al. (2001) Ligand-induced Dynamic Membrane Changes and Cell Deletion Conferred by Vanilloid Receptor 1. J Biol Chem 276: 11021-11030.
2. Liu, M, Liu MC, Magoulas C, Priestley JV, Willmott NJ (2003) Versatile regulation of cytosolic Ca2+ by vanilloid receptor I in rat dorsal root ganglion neurons. J Biol Chem 278: 5462-5472.
3. Marshall IC, Owen DE, Cripps TV, Davis JB, McNulty S, et al. (2003) Activation of vanilloid receptor 1 by resiniferatoxin mobilizes calcium from inositol 1,4,5-trisphosphate-sensitive stores. Br J Pharmacol 138: 172-176.
4. Karai L, Russell JT, Iadarola MJ, Olah Z (2004) Vanilloid receptor I regulates multiple calcium compartments and contributes to Ca2+-induced Ca2+-release in sensory neuronsn. J Biol Chem.
5. Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sorgard M, et al. (1999) Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400: 452-457.
6. Olah Z, Karai L, Iadarola MJ (2001) Anandamide Activates Vanilloid Receptor 1 (VR1) at Acidic pH in Dorsal Root Ganglia Neurons and Cells Ectopically Expressing VR1. J Biol Chem 276: 31163-31170.
7. Jordt SE, Tominaga M, Julius D (2000) Acid potentiation of the capsaicin receptor determined by a key extracellular site. Proc Natl Acad Sci U S A 97: 8134-8139.
8. Vellani V, Mapplebeck S, Moriondo A, Davis JB, McNaughton PA (2001) Protein kinase C activation potentiates gating of the vanilloid receptor VR1 by capsaicin, protons, heat and anandamide. J Physiol 534: 813-825.
9. Premkumar LS, Ahern GP (2000) Induction of vanilloid receptor channel activity by protein kinase C. Natutre 408: 985-990.
10. Olah Z, Karai L, Iadarola MJ (2002) Protein Kinase Calpha is Required for Vanilloid Receptor 1 Activation. EVIDENCE FOR MULTIPLE SIGNALING PATHWAYS. J Biol Chem 277: 35752-35759.
11. Jung J, Shin JS, Lee SY, Hwang SW, Koo J, et al. (2003) Phosphorylation of vanilloid receptor 1 by Ca+2/calmodulin-dependent kinase II regulates its vanilloid binding. J Biol Chem.
12. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, et al. (1998) The cloned capsaicin receptor integrates multiple pain-producing stimuli Neuron 21: 531-543.
13. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, et al. (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824.
14. Bhave G, Hu HJ, Glauner KS, Zhu W, Wang H, et al. (2003) Protein kinase C phosphorylation sensitizes but does not activate the capsaicin receptor transient receptor potential vanilloid 1 (TRPV1). Proc Natl Acad Sci U S A 100: 12480-12485.
15. Jordt SE, Julius D (2002) Molecular basis for species-specific sensitivity to "hot" chili peppers. Cell 108: 421-430.
16. Kedei N, Szabo t, Lile JD, Treanor JJ, Olah Z, et al. (2001) Analysis of the native quaternary structure of vanilloid receptor 1. J Biol Chem 276: 28613-28619.
17. Donato R (1999) Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type. Biochim Biophys Acta 1450: 191-231.
18. Likic VA, Gooley PR, Speed TP, Strehler EE (2005) A statistical approach to the interpretation of molecular dynamics simulations of calmodulin equilibrium dynamics. Protein Sci 14: 2955-2963.
19. Douglass PM, Salins LL, Dikici E, Daunert S (2002) Class-selective drug detection: fluorescently-labeled calmodulin as the biorecognition element for phenothiazines and tricyclic antidepressants. Bioconjug Chem 13: 1186-1192.
20. Slemmon JR, Morgan JI, Fullerton SM, Danho W, Hilbush BS, et al. (1996) Camstatins are peptide antagonists of calmodulin based upon a conserved structural motif in PEP-19, neurogranin, and neuromodulin. J Biol Chem 271: 15911-15917.
21. Johanson RA, Sarau HM, Foley JJ, Slemmon JR (2000) Calmodulin-binding peptide PEP-19 modulates activation of calmodulin kinase II In situ. J Neurosci 20: 2860-2866.
22. Rosenbaum T, Gordon-Shaag A, Munari M, Gordon SE (2004) Ca2+/Calmodulin Modulates TRPV1 Activation by Capsaicin. J Gen Physiol 123: 53-62.
23. Numazaki M, Tominaga T, Takeuchi K, Murayama N, Toyooka H, et al. (2003) Structural determinant of TRPV1 desensitization interacts with calmodulin. Proc Natl Acad Sci U S A 100: 8002-8006.
24. Zhang Z, Tang J, Tikunova S, Johnson JD, Chen Z, et al. (2001) Activation of Trp3 by inositol 1,4,5-trisphosphate receptors through displacement of inhibitory calmodulin from a common binding domain. Proc Natl Acad Sci U S A 98: 3168-3173.
25. Tang J, Lin Y, Zhang Z, Tikunova S, Birnbaumer L, et al. (2001) Identification of common binding sites for calmodulin and inositol 1,4,5-trisphosphate receptors on the carboxyl termini of trp channels. J Biol Chem 276: 21303-21310.
26. Harper JL, Daly JW (2000) Effect of calmidazolium analogs on calcium influx in HL-60 cells. Biochem Pharmacol 60: 317-324.
27. Gamper N, Shapiro MS (2003) Calmodulin mediates Ca2+-dependent modulation of M-type K+ channels. J Gen Physiol 122: 17-31.
28. Bruening-Wright A, Schumacher MA, Adelman JP, Maylie J (2002) Localization of the activation gate for small conductance Ca2+-acdvated K+ channels. J Neurosci 22: 6499-6506.
29. Soldatov NM (2003) Ca2+ channel moving tail: link between Ca2+-induced inactivation and Ca2+ signal transduction. Trends Pharmacol Sci 24: 167-171.
30. Boulay G (2002) Ca(2+)-calmodulin regulates receptor-operated Ca(2+) entry activity of TRPC6 in HEK-293 cells. Cell Calcium 32: 201-207.
31. Rigden DJ, Jedrzejas MJ, Galperin MY (2003) An extracellular calcium-binding domain in bacteria with a distant relationship to EF-hands. FEMS Microbiol Lett 221: 103-110.
32. Menendez L, Perez-Vallina JR, Cantabrana B, Hidalgo A, Baamonde A (1996) Calmodulin inhibitors induce spinal analgesia in rats. Brain Res 731: 114-121.
33. Williams M, Kowaluk EA, Arneric SP (1999) Emerging molecular approaches to pain therapy. J Med Chem 42: 1481-1500.
34. Acs G, Palkovits M, Blumberg PM (1995) Trifluoperazine modulates [3H]resiniferatoxin binding by human and rat vanilloid (capsaicin) receptors and affects 45Ca uptake by adult rat dorsal root ganglion neurones. J Pharmacol Exp Ther 274: 1090-1098.
35. Jung J, Hwang SW, Kwak J, Lee SY, Kang CJ, et al. (1999) Capsaiein binds to the intracellular domain of the capsaicin-activated ion channel. J Neurosci 19: 529-538.
36. Robinson LR, Czerniecki JM, Ehde DM, Edwards WT, Judish DA, et al. (2004) Trial of amitriptyline for refief of pain in amputees: results of a randomized controlled study. Arch Phys Med Rehabil 85: 1-6.
37. Max MB (1994) Treatment of post-herpetic neuralgia: antidepressants. Ann Neurol 35 Suppl; S50-53.
38. Kieburtz K, Simpson D, Yiannoutsos C, Max MB, Hall CD, et al. (1998) A randomized trial of amitrptyline and mexiletine for painful neuropathy in HIV infection. AIDS Clinical Trial Group 242 Protocol Team. Neurology 51: 1682-1688.
39. Khoromi S, Cui L, Nackers L, Max MB (2006) Morphine, nortriptyline and their combination vs. placebo in patients with chronic lumbar root pain. Pain.
40. Jorgensen WL (2004) The many roles of computation in drug discovery. Science 303: 1813-1818.
41. Fang L, Wu J, Lin Q, Willis WD (2002) Calcium-calmodulin-dependent protein kinase II contributes to spinal cord central sensitization. J Neurosci 22: 4196-4204.
42. Olah Z, Szabo T, Karai L, Hough C, Fields RD, et al. (2001) Ligand-inchiced dynamic membrane changes and cell deletion conferred by vanilloid receptor 1. J Biol Chem 276: 11021-11030.
43. Karai LJ, Russell JT, Iadarola MJ, Olah Z (2004) Vanilloid receptor 1 regulates multiple calcium compartments and contributes to Ca2+-induced Ca2+ release in sensory neurons. J Biol Chem 279: 16377-16387.
44. Mohapatra DP, Wang SY, Wang GK. Nan C (2003) A tyrosine residue in TM6 of the Vanilloid Receptor TRPV1 involved in desensitization and calcium permeability of capsaicin-activated currents. Mol Cell Neurosci 23: 314-324.
45. Garcia-Martinez C, Morenilla-Palao C, Planells-Cases R, Merino JM, Ferrer-Montiel A (2000) Identification of an aspartic residue in the P loop of the vanilloid receptor that modulates pore properties. J Biol Chem 275: 32552-32558.
46. Kitaguchi T, Swartz KJ (2005) An inhibitor of TRPV1 channels isolated from funnel Web spider venom. Biochemistry 44: 15544-15549.
47. Del Carlo B, Pellegrini M, Pellegrino M (2002) Calmodulin antagonists do not inhibit IK(Ca) channels of human erythrocytes. Biochim Biophys Acta 1558: 133-141.
48. Brown DC, Iadarola MJ, Perkowski SZ, Erin H, Shofer F, et al. (2005) Physiologic and antinociceptive effects of intrathecal resiniferatoxin in a canine bone cancer model. Anesthesiology 103: 1052-1059.
49. Karai L, Brown DC, Mannes AJ, Connelly ST, Brown J, et al. (2004) Deletion of vanilloid receptor 1-expressing primary afferent neurons for pain control. J Clin Invest 113: 1344-1352.
50. Tender GC, Walbridge S, Olah Z, Karai L, Iadarola M, et al. (2005) Selective ablation of nociceptive neurons for elimination of hyperalgesia and neurogenic inflammation. J Neurosurg 102: 522-525.
51. Peitsch MC (1995) Protein modeling by e-mail. Bio/Technology 13: 658-660.
52. Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18: 2714-2723.
53. Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Res 31: 3381-3385.
54. Boeckmann B, Bairoch A, Apweiler R, Blatter MC, Estreicher A, et al. (2003) The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res 31: 365-370.
55. Krogh A, Larsson B, von Heijrie G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580.
56. Zhout Y, Morais-Cabral JH, Kaufman A, MacKinnon R (2001) Chemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0 A resolution. Nature 414: 43-48.
57. van Gunsteren WF (1996) Biomolecular simulation: the GROMOS96 manual and user guide. Vdf Hochschulverlag, ETHZ.
58. Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14: 33-38, 27-38.