Polypeptide modulators of TRPV1 produce analgesia without hyperthermia

Marine Drugs

Volumn 11, Issue 12, 2013, Pages 5100-5115

  Andreev, Yaroslav A ^a   Kozlov, Sergey A ^a   Korolkova, Yuliya V ^a   Dyachenko, Igor A ^a,b   Bondarenko, Dmitrii A ^a,b   Skobtsov, Denis I ^a   Murashev, Arkadii N ^a,b   Kotova, Polina D ^c   Rogachevskaja, Olga A ^c   Kabanova, Natalia V ^c   Kolesnikov, Stanislav S ^c   Grishin, Eugene V ^a  

^a SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^b PUSHCHINO STATE UNIVERSITY   (Russian Federation)

^c INSTITUTE OF CELL BIOPHYSICS   (Russian Federation)

Author keywords

Analgesic polypeptide APHC; Animal models; Inflammation; Nociception; Sea anemone; Temperature regulation; TRPV1 receptor

Indexed keywords

ANALGESIC AGENT; CALCIUM ION; CAPSAICIN; POLYPEPTIDE; PROTEIN APHC1; PROTEIN APHC3; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; VANILLOID RECEPTOR 1 ANTAGONIST;

ADULT; ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINOCICEPTION; ARTICLE; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; CORE TEMPERATURE; DRUG EFFICACY; HOT PLATE TEST; HUMAN; HUMAN CELL; HYPERALGESIA; HYPERTHERMIA; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; INFLAMMATORY PAIN; LATENT PERIOD; MALE; MOUSE; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; PAIN; PATCH CLAMP TECHNIQUE; PH; RECEPTOR BLOCKING; TEMPERATURE SENSITIVITY; TREATMENT RESPONSE; WRITHING TEST;

ANALGESIA; ANALGESICS; ANIMALS; BODY TEMPERATURE; CAPSAICIN; CELL LINE; DISEASE MODELS, ANIMAL; FEVER; HEK293 CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; HYPERALGESIA; INFLAMMATION; MALE; MICE; PAIN; PEPTIDES; TRPV CATION CHANNELS;

EID: 84892393861     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md11125100     Document Type: Article

References (37)

1. Caterina, M.J.; Leffler, A.; Malmberg, A.B.; Martin, W.J.; Trafton, J.; Petersen-Zeitz, K.R.; Koltzenburg, M.; Basbaum, A.I.; Julius, D. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 2000, 288, 306-313.
2. Caterina, M.J.; Schumacher, M.A.; Tominaga, M.; Rosen, T.A.; Levine, J.D.; Julius, D. The capsaicin receptor: A heat-activated ion channel in the pain pathway. Nature 1997, 389, 816-824.
3. Tominaga, M.; Caterina, M.J.; Malmberg, A.B.; Rosen, T.A.; Gilbert, H.; Skinner, K.; Raumann, B.E.; Basbaum, A.I.; Julius, D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 1998, 21, 531-543.
4. Szallasi, A.; Cortright, D.N.; Blum, C.A.; Eid, S.R. The vanilloid receptor TRPV1: 10 years from channel cloning to antagonist proof-of-concept. Nat. Rev. Drug Discov. 2007, 6, 357-372.
5. Malmberg, A.; Bley, K. Turning Up the Heat on Pain: TRPV1 Receptors in Pain and Inflammation; Birkhauser Verlag: Basel, Boston, Berlin, 2005.
6. Szallasi, A.; Appendino, G. Vanilloid receptor TRPV1 antagonists as the next generation of painkillers. Are we putting the cart before the horse? J. Med. Chem. 2004, 47, 2717-2723.
7. Gunthorpe, M.J.; Chizh, B.A. Clinical development of TRPV1 antagonists: Targeting a pivotal point in the pain pathway. Drug Discov. Today 2009, 14, 56-67.
8. Gavva, N.R.; Bannon, A.W.; Surapaneni, S.; Hovland, D.N., Jr.; Lehto, S.G.; Gore, A.; Juan, T.; Deng, H.; Han, B.; Klionsky, L.; et al. The vanilloid receptor TRPV1 is tonically activated in vivo and involved in body temperature regulation. J. Neurosci. 2007, 27, 3366-3374.
9. Gavva, N.R.; Treanor, J.J.; Garami, A.; Fang, L.; Surapaneni, S.; Akrami, A.; Alvarez, F.; Bak, A.; Darling, M.; Gore, A.; et al. Pharmacological blockade of the vanilloid receptor TRPV1 elicits marked hyperthermia in humans. Pain 2008, 136, 202-210.
10. Honore, P.; Chandran, P.; Hernandez, G.; Gauvin, D.M.; Mikusa, J.P.; Zhong, C.; Joshi, S.K.; Ghilardi, J.R.; Sevcik, M.A.; Fryer, R.M.; et al. Repeated dosing of ABT-102, a potent and selective TRPV1 antagonist, enhances TRPV1-mediated analgesic activity in rodents, but attenuates antagonist-induced hyperthermia. Pain 2009, 142, 27-35.
11. Immke, D.C.; Gavva, N.R. The TRPV1 receptor and nociception. Semin. Cell Dev. Biol. 2006, 17, 582-591.
12. Lehto, S.G.; Tamir, R.; Deng, H.; Klionsky, L.; Kuang, R.; Le, A.; Lee, D.; Louis, J.C.; Magal, E.; Manning, B.H.; et al. Antihyperalgesic effects of (R,E)-N-(2-hydroxy-2,3-dihydro-1H-inden-4-yl)-3-(2-(piperidin-1-yl) -4-(trifluorom ethyl)phenyl)-acrylamide (AMG8562), a novel transient receptor potential vanilloid type 1 modulator that does not cause hyperthermia in rats. J. Pharmacol. Exp. Ther. 2008, 326, 218-229.
13. Garami, A.; Shimansky, Y.P.; Pakai, E.; Oliveira, D.L.; Gavva, N.R.; Romanovsky, A.A. Contributions of different modes of TRPV1 activation to TRPV1 antagonist-induced hyperthermia. J. Neurosci. 2010, 30, 1435-1440.
14. Andreev, Y.A.; Kozlov, S.A.; Koshelev, S.G.; Ivanova, E.A.; Monastyrnaya, M.M.; Kozlovskaya, E.P.; Grishin, E.V. Analgesic compound from sea anemone Heteractis crispa is the first polypeptide inhibitor of vanilloid receptor 1 (TRPV1). J. Biol. Chem. 2008, 283, 23914-23921.
15. Andreev, Y.A.; Kozlov, S.A.; Kozlovskaya, E.P.; Grishin, E.V. Analgesic effect of a polypeptide inhibitor of the TRPV1 receptor in noxious heat pain models. Dok. Biochem. Biophys. 2009, 424, 46-48.
16. Kozlov, S.A.; Andreev, Y.A.; Murashev, A.N.; Skobtsov, D.I.; D'yachenko, I.A.; Grishin, E.V. New polypeptide components from the Heteractis crispa sea anemone with analgesic activity. Russ. J. Bioorgan. Chem. 2009, 35, 711-719.
17. Philyppov, I.B.; Paduraru, O.N.; Andreev, Y.A.; Grishin, E.V.; Shuba, Y.M. Modulation of TRPV1-dependent contractility of normal and diabetic bladder smooth muscle by analgesic toxins from sea anemone Heteractis crispa. Life Sci. 2012, 91, 912-920.
18. Kozlov, S.; Grishin, E. Convenient nomenclature of cysteine-rich polypeptide toxins from sea anemones. Peptides 2012, 33, 240-244.
19. Antuch, W.; Berndt, K.D.; Chavez, M.A.; Delfin, J.; Wuthrich, K. The NMR solution structure of a Kunitz-type proteinase inhibitor from the sea anemone Stichodactyla helianthus. Eur. J. Biochem. 1993, 212, 675-684.
20. Gebhard, W.; Tschesche, H.; Fritz, H. Biochemistry of aprotinin and aprotinin-like inhibitors. In Proteinase Inhibitors; Barrett, A.J., Salvesen, G., Eds.; Elsevier: Amsterdam, The Netherlands, 1986; pp. 375-388.
21. Creighton, T.E.; Charles, I.G. Sequences of the genes and polypeptide precursors for two bovine protease inhibitors. J. Mol. Biol. 1987, 194, 11-22.
22. Siemens, J.; Zhou, S.; Piskorowski, R.; Nikai, T.; Lumpkin, E.A.; Basbaum, A.I.; King, D.; Julius, D. Spider toxins activate the capsaicin receptor to produce inflammatory pain. Nature 2006, 444, 208-212.
23. Bohlen, C.J.; Priel, A.; Zhou, S.; King, D.; Siemens, J.; Julius, D. A bivalent tarantula toxin activates the capsaicin receptor, TRPV1, by targeting the outer pore domain. Cell 2010, 141, 834-845.
24. Klionsky, L.; Tamir, R.; Holzinger, B.; Bi, X.; Talvenheimo, J.; Kim, H.; Martin, F.; Louis, J.C.; Treanor, J.J.; Gavva, N.R. A polyclonal antibody to the prepore loop of transient receptor potential vanilloid type 1 blocks channel activation. J. Pharmacol. Exp. Ther. 2006, 319, 192-198.
25. McNamara, C.R.; Mandel-Brehm, J.; Bautista, D.M.; Siemens, J.; Deranian, K.L.; Zhao, M.; Hayward, N.J.; Chong, J.A.; Julius, D.; Moran, M.M.; et al. TRPA1 mediates formalin-induced pain. Proc. Natl. Acad. Sci. USA 2007, 104, 13525-13530.
26. Le Bars, D.; Gozariu, M.; Cadden, S.W. Animal models of nociception. Pharmacol. Rev. 2001, 53, 597-652.
27. Tang, L.; Chen, Y.; Chen, Z.; Blumberg, P.M.; Kozikowski, A.P.; Wang, Z.J. Antinociceptive pharmacology of N-(4-chlorobenzyl)-N′-(4-hydroxy-3- iodo-5-methoxybenzyl) thiourea, a high-affinity competitive antagonist of the transient receptor potential vanilloid 1 receptor. J. Pharmacol. Exp. Ther. 2007, 321, 791-798.
28. Staruschenko, A.; Jeske, N.A.; Akopian, A.N. Contribution of TRPV1-TRPA1 interaction to the single channel properties of the TRPA1 channel. J. Biol. Chem. 2010, 285, 15167-15177.
29. Davis, J.B.; Gray, J.; Gunthorpe, M.J.; Hatcher, J.P.; Davey, P.T.; Overend, P.; Harries, M.H.; Latcham, J.; Clapham, C.; Atkinson, K.; et al. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 2000, 405, 183-187.
30. Jara-Oseguera, A.; Simon, S.A.; Rosenbaum, T. TRPV1: On the road to pain relief. Curr. Mol. Pharmacol. 2008, 1, 255-269.
31. Ikeda, Y.; Ueno, A.; Naraba, H.; Oh-ishi, S. Involvement of vanilloid receptor VR1 and prostanoids in the acid-induced writhing responses of mice. Life Sci. 2001, 69, 2911-2919.
32. Romanovsky, A.A.; Almeida, M.C.; Garami, A.; Steiner, A.A.; Norman, M.H.; Morrison, S.F.; Nakamura, K.; Burmeister, J.J.; Nucci, T.B. The transient receptor potential vanilloid-1 channel in thermoregulation: A thermosensor it is not. Pharmacol. Rev. 2009, 61, 228-261.
33. Steiner, A.A.; Turek, V.F.; Almeida, M.C.; Burmeister, J.J.; Oliveira, D.L.; Roberts, J.L.; Bannon, A.W.; Norman, M.H.; Louis, J.C.; Treanor, J.J.; et al. Nonthermal activation of transient receptor potential vanilloid-1 channels in abdominal viscera tonically inhibits autonomic cold-defense effectors. J. Neurosci. 2007, 27, 7459-7468.
34. Fosgerau, K.; Weber, U.J.; Gotfredsen, J.W.; Jayatissa, M.; Buus, C.; Kristensen, N.B.; Vestergaard, M.; Teschendorf, P.; Schneider, A.; Hansen, P.; et al. Drug-induced mild therapeutic hypothermia obtained by administration of a transient receptor potential vanilloid type 1 agonist. BMC Cardiovasc. Disord. 2010, 10, 51.
35. Andreev, Y.A.; Kozlov, S.A.; Vassilevski, A.A.; Grishin, E.V. Cyanogen bromide cleavage of proteins in salt and buffer solutions. Anal. Biochem. 2010, 407, 144-146.
36. Sakurada, T.; Katsumata, K.; Tan-No, K.; Sakurada, S.; Kisara, K. The capsaicin test in mice for evaluating tachykinin antagonists in the spinal cord. Neuropharmacology 1992, 31, 1279-1285.
37. Tjolsen, A.; Berge, O.G.; Hunskaar, S.; Rosland, J.H.; Hole, K. The formalin test: An evaluation of the method. Pain 1992, 51, 5-17.