Structural determinants of the transient receptor potential 1 (TRPV1) channel activation by phospholipid analogs

Journal of Biological Chemistry

Volumn 289, Issue 35, 2014, Pages 24079-24090

  Morales Lázaro, Sara L ^a   Serrano Flores, Barbara ^a   Llorente, Itzel ^a   Hernández García, Enrique ^a   González Ramírez, Ricardo ^b   Banerjee, Souvik ^c   Miller, Duane ^c   Gududuru, Veeresh ^d   Fells, James ^c   Norman, Derek ^c   Tigyi, Gabor ^c   Escalante Alcalde, Diana ^a   Rosenbaum, Tamara ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b HOSPITAL GENERAL DR MANUEL GEA GONZÁLEZ   (Mexico)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^d RxBio Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOLS; CHEMICAL ACTIVATION; CHEMICAL BONDS; ENZYME ACTIVITY; PROTEINS;

CONFORMATIONAL CHANGE; G PROTEIN COUPLED RECEPTORS; LYSOPHOSPHATIDIC ACID; MECHANISTIC MODELING; STRUCTURAL DETERMINANTS; STRUCTURAL REQUIREMENTS; TRANSIENT RECEPTOR POTENTIAL VANILLOID; TRANSIENT RECEPTOR POTENTIALS;

PHOSPHOLIPIDS;

CAPSAICIN; G PROTEIN COUPLED RECEPTOR; HYDROCARBON; LYSOPHOSPHATIDIC ACID; PHOSPHATE; PHOSPHOLIPID DERIVATIVE; PHOSPHOROTHIOIC ACID; VANILLOID RECEPTOR 1; LYSOPHOSPHOLIPID; TRPV1 PROTEIN, HUMAN; VANILLOID RECEPTOR;

ARTICLE; CHANNEL GATING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; HEK293 CELL LINE; HUMAN; HUMAN CELL; PHARMACOPHORE; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; STRUCTURE ACTIVITY RELATION; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN CONFORMATION;

HEK293 CELLS; HUMANS; LYSOPHOSPHOLIPIDS; MODELS, MOLECULAR; PROTEIN CONFORMATION; TRPV CATION CHANNELS;

EID: 84906871292     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.572503     Document Type: Article

References (48)

1. Vay, L., Gu, C., and McNaughton, P. A. (2012) The thermo-TRP ion channel family: properties and therapeutic implications. Br. J. Pharmacol. 165, 787-801
2. Moran, M. M., McAlexander, M. A., Bíró, T., and Szallasi, A. (2011) Transient receptor potential channels as therapeutic targets. Nat. Rev. Drug Discov. 10, 601-620
3. Engler, A., Aeschlimann, A., Simmen, B. R., Michel, B. A., Gay, R. E., Gay, S., and Sprott, H. (2007) Expression of transient receptor potential vanilloid 1 (TRPV1) in synovial fibroblasts from patients with osteoarthritis and rheumatoid arthritis. Biochem. Biophys. Res. Commun. 359, 884-888 (Pubitemid 46957540)
4. Pan, H. L., Zhang, Y. Q., and Zhao, Z. Q. (2010) Involvement of lysophosphatidic acid in bone cancer pain by potentiation of TRPV1 via PKCε pathway in dorsal root ganglion neurons. Mol. Pain 6, 85
5. Sadofsky, L. R., Ramachandran, R., Crow, C., Cowen, M., Compton, S. J., and Morice, A. H. (2012) Inflammatory stimuli up-regulate transient receptor potential vanilloid-1 expression in human bronchial fibroblasts. Exp. Lung Res. 38, 75-81
6. Caterina, M. J., Schumacher, M. A., Tominaga, M., Rosen, T. A., Levine, J. D., and Julius, D. (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816-824 (Pubitemid 27462969)
7. Hwang, S. W., Cho, H., Kwak, J., Lee, S. Y., Kang, C. J., Jung, J., Cho, S., Min, K. H., Suh, Y. G., Kim, D., and Oh, U. (2000) Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances. Proc. Natl. Acad. Sci. U.S.A. 97, 6155-6160 (Pubitemid 30367539)
8. Morales-Lázaro, S. L., Simon, S. A., and Rosenbaum, T. (2013) The role of endogenous molecules in modulating pain through transient receptor potential vanilloid 1 (TRPV1). J. Physiol. 591, 3109-3121
9. Nieto-Posadas, A., Picazo-Juárez, G., Llorente, I., Jara-Oseguera, A., Morales-Lázaro, S., Escalante-Alcalde, D., Islas, L. D., and Rosenbaum, T. (2012) Lysophosphatidic acid directly activates TRPV1 through a C-terminal binding site. Nat. Chem. Biol. 8, 78-85
10. Lin, M. E., Herr, D. R., and Chun, J. (2010) Lysophosphatidic acid (LPA) receptors: signaling properties and disease relevance. Prostaglandins Other Lipid Mediat. 91, 130-138
11. Baker, D. L., Desiderio, D. M., Miller, D. D., Tolley, B., and Tigyi, G. J. (2001) Direct quantitative analysis of lysophosphatidic acid molecular species by stable isotope dilution electrospray ionization liquid chromatography-mass spectrometry. Anal. Biochem. 292, 287-295
12. Choi, J. W., Herr, D. R., Noguchi, K., Yung, Y. C., Lee, C. W., Mutoh, T., Lin, M. E., Teo, S. T., Park, K. E., Mosley, A. N., and Chun, J. (2010) LPA receptors: subtypes and biological actions. Annu. Rev. Pharmacol. Toxicol. 50, 157-186
13. Ueda, H., Matsunaga, H., Olaposi, O. I., and Nagai, J. (2013) Lysophosphatidic acid: chemical signature of neuropathic pain. Biochim. Biophys. Acta 1831, 61-73
14. Inoue, M., Rashid, M. H., Fujita, R., Contos, J. J., Chun, J., and Ueda, H. (2004) Initiation of neuropathic pain requires lysophosphatidic acid receptor signaling. Nat. Med. 10, 712-718 (Pubitemid 38937636)
15. Lukacs, V., Thyagarajan, B., Varnai, P., Balla, A., Balla, T., and Rohacs, T. (2007) Dual regulation of TRPV1 by phosphoinositides. J. Neurosci. 27, 7070-7080 (Pubitemid 47015892)
16. Lukacs, V., Rives, J. M., Sun, X., Zakharian, E., and Rohacs, T. (2013) Promiscuous activation of transient receptor potential vanilloid 1 (TRPV1) channels by negatively charged intracellular lipids: the key role of endogenous phosphoinositides in maintaining channel activity. J. Biol. Chem. 288, 35003-35013
17. Ufret-Vincenty, C. A., Klein, R. M., Hua, L., Angueyra, J., and Gordon, S. E. (2011) Localization of the PIP2 sensor of TRPV1 ion channels. J. Biol. Chem. 286, 9688-9698
18. Senning, E. N., Collins, M. D., Stratiievska, A., Ufret-Vincenty, C. A., and Gordon, S. E. (2014) Regulation of TRPV1 by phosphoinositide (4,5)-bisphosphate: role of membrane asymmetry. J. Biol. Chem. 289, 10999-11006
19. Cao, E., Cordero-Morales, J. F., Liu, B., Qin, F., and Julius, D. (2013) TRPV1 channels are intrinsically heat sensitive and negatively regulated by phosphoinositide lipids. Neuron 77, 667-679
20. Stein, A. T., Ufret-Vincenty, C. A., Hua, L., Santana, L. F., and Gordon, S. E. (2006) Phosphoinositide 3-kinase binds to TRPV1 and mediates NGF-stimulated TRPV1 trafficking to the plasma membrane. J. Gen. Physiol. 128, 509-522 (Pubitemid 44664629)
21. Klein, R. M., Ufret-Vincenty, C. A., Hua, L., and Gordon, S. E. (2008) Determinants of molecular specificity in phosphoinositide regulation. Phosphatidylinositol (4,5)-bisphosphate (PI(4,5)P2) is the endogenous lipid regulating TRPV1. J. Biol. Chem. 283, 26208-26216
22. Telezhkin, V., Reilly, J. M., Thomas, A. M., Tinker, A., and Brown, D. A. (2012) Structural requirements of membrane phospholipids for Mtype potassium channel activation and binding. J. Biol. Chem. 287, 10001-10012
23. Telezhkin, V., Brown, D. A., and Gibb, A. J. (2012) Distinct subunit contributions to the activation of M-type potassium channels by PI(4,5)P2. J. Gen. Physiol. 140, 41-53
24. Gududuru, V. (April 1, 2014) U. S. Patent 8, 686,177 B2
25. Durgam, G. G., Virag, T., Walker, M. D., Tsukahara, R., Yasuda, S., Liliom, K., van Meeteren, L. A., Moolenaar, W. H., Wilke, N., Siess, W., Tigyi, G., and Miller, D. D. (2005) Synthesis, structure-activity relationships, and biological evaluation of fatty alcohol phosphates as lysophosphatidic acid receptor ligands, activators of PPARγ, and inhibitors of autotaxin. J. Med. Chem. 48, 4919-4930 (Pubitemid 41033134)
26. Rosenbaum, T., and Gordon, S. E. (2002) Dissecting intersubunit contacts in cyclic nucleotide-gated ion channels. Neuron 33, 703-713 (Pubitemid 34219242)
27. Movahed, P., Jönsson, B. A., Birnir, B., Wingstrand, J. A., Jørgensen, T. D., Ermund, A., Sterner, O., Zygmunt, P. M., and Högestätt, E. D. (2005) Endogenous unsaturated C18 N-acylethanolamines are vanilloid receptor (TRPV1) agonists. J. Biol. Chem. 280, 38496-38504 (Pubitemid 43853748)
28. Brauchi, S., Orta, G., Mascayano, C., Salazar, M., Raddatz, N., Urbina, H., Rosenmann, E., Gonzalez-Nilo, F., and Latorre, R. (2007) Dissection of the components for PIP2 activation and thermosensation in TRP channels. Proc. Natl. Acad. Sci. U.S.A. 104, 10246-10251 (Pubitemid 47175294)
29. Huey, R., Morris, G. M., Olson, A. J., and Goodsell, D. S. (2007) A semiempirical free energy force field with charge-based desolvation. J. Comput. Chem. 28, 1145-1152 (Pubitemid 46506716)
30. Seeliger, D., and de Groot, B. L. (2010) Ligand docking and binding site analysis with PyMOL and Autodock/Vina. J. Comput. Aided Mol. Des. 24, 417-422
31. Kobayashi, T., Tanaka-Ishii, R., Taguchi, R., Ikezawa, H., and Murakami- Murofushi, K. (1999) Existence of a bioactive lipid, cyclic phosphatidic acid, bound to human serum albumin. Life Sci. 65, 2185-2191 (Pubitemid 29524868)
32. van Schooten, B., Testerink, C., and Munnik, T. (2006) Signalling diacylglycerol pyrophosphate, a new phosphatidic acid metabolite. Biochim. Biophys. Acta 1761, 151-159
33. Wissing, J. B., and Behrbohm, H. (1993) Diacylglycerol pyrophosphate, a novel phospholipid compound. FEBS Lett. 315, 95-99 (Pubitemid 23005739)
34. Oshiro, J., Han, G. S., and Carman, G. M. (2003) Diacylglycerol pyrophosphate phosphatase in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1635, 1-9 (Pubitemid 37464990)
35. Martinez-Seara, H., Róg, T., Pasenkiewicz-Gierula, M., Vattulainen, I., Karttunen, M., and Reigada, R. (2007) Effect of double bond position on lipid bilayer properties: insight through atomistic simulations. J. Phys. Chem. B 111, 11162-11168 (Pubitemid 47554246)
36. Xu, X., Yang, G., Zhang, H., and Prestwich, G. D. (2009) Evaluating dual activity LPA receptor pan-antagonist/autotaxin inhibitors as anti-cancer agents in vivo using engineered human tumors. Prostaglandins Other Lipid Mediat. 89, 140-146
37. Tsukahara, T., Tsukahara, R., Fujiwara, Y., Yue, J., Cheng, Y., Guo, H., Bolen, A., Zhang, C., Balazs, L., Re, F., Du, G., Frohman, M. A., Baker, D. L., Parrill, A. L., Uchiyama, A., Kobayashi, T., Murakami-Murofushi, K., and Tigyi, G. (2010) Phospholipase D2-dependent inhibition of the nuclear hormone receptor PPARγ by cyclic phosphatidic acid. Mol. Cell 39, 421-432
38. Kakiuchi, Y., Nagai, J., Gotoh, M., Hotta, H., Murofushi, H., Ogawa, T., Ueda, H., and Murakami-Murofushi, K. (2011) Antinociceptive effect of cyclic phosphatidic acid and its derivative on animal models of acute and chronic pain. Mol. Pain 7, 33
39. Liu, G. X., Hanley, P. J., Ray, J., and Daut, J. (2001) Long-chain acyl-coenzyme A esters and fatty acids directly link metabolism to K(ATP) channels in the heart. Circ. Res. 88, 918-924 (Pubitemid 32441470)
40. + channels. Proc. Natl. Acad. Sci. U.S.A. 110, 4816-4821
41. Rohács, T., Lopes, C. M., Jin, T., Ramdya, P. P., Molnár, Z., and Logothetis, D. E. (2003) Specificity of activation by phosphoinositides determines lipid regulation of Kir channels. Proc. Natl. Acad. Sci. U.S.A. 100, 745-750 (Pubitemid 36126123)
42. Perillo, V. L., Fernández-Nievas, G. A., Vallés, A. S., Barrantes, F. J., and Antollini, S. S. (2012) The position of the double bond in monounsaturated free fatty acids is essential for the inhibition of the nicotinic acetylcholine receptor. Biochim. Biophys. Acta 1818, 2511-2520
43. Bartlett, G. J., Choudhary, A., Raines, R. T., and Woolfson, D. N. (2010) n→π* interactions in proteins. Nat. Chem. Biol. 6, 615-620
44. Rosenbaum, T., and Simon, S. A. (2007) in TRP Ion Channel Function in Sensory Transduction and Cellular Signaling Cascades (Liedtke, W. B., and Heller, S., eds) pp. 69-84, CRC Press, Inc., Boca Raton, FL
45. Ma, L., Nagai, J., Chun, J., and Ueda, H. (2013) An LPA species (18:1 LPA) plays key roles in the self-amplification of spinal LPA production in the peripheral neuropathic pain model. Mol. Pain 9, 29
46. + channel Kir2.2. Nature 477, 495-498
47. Cao, E., Liao, M., Cheng, Y., and Julius, D. (2013) TRPV1 structures in distinct conformations reveal activation mechanisms. Nature 504, 113-118
48. Cheng, W. W., D'Avanzo, N., Doyle, D. A., and Nichols, C. G. (2011) Dual-mode phospholipid regulation of human inward rectifying potassium channels. Biophys. J. 100, 620-628