Phosphatidylinositol-4,5-biphosphate-dependent rearrangement of TRPV4 cytosolic tails enables channel activation by physiological stimuli

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 23, 2013, Pages 9553-9558

  Garcia Elias, Anna ^a   Mrkonjić, Sanela ^a   Pardo Pastor, Carlos ^a   Inada, Hitoshi ^b   Hellmich, Ute A ^b   Rubio Moscardó, Fanny ^a   Plata, Cristina ^a   Gaudet, Rachelle ^b   Vicente, Rubén ^a   Valverde, Miguel A ^a  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b HARVARD UNIVERSITY   (United States)

Author keywords

Regulation; Structure; Thermosensitivity

Indexed keywords

4ALPHA PHORBOL DIDECANOATE; 5,6 EPOXY 8,11,14 ICOSATRIENOIC ACID; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOLIPASE C; POTASSIUM CHANNEL; PROTEIN KINASE C; VANILLOID RECEPTOR 4;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CELL MEMBRANE; CELL SWELLING; CONTROLLED STUDY; CYTOSOL; EPITHELIUM CELL; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEAT; MOUSE; MUSCLE HYPOTONIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

REGULATION; STRUCTURE; THERMOSENSITIVITY;

ANALYSIS OF VARIANCE; CALCIUM; CELLS, CULTURED; CLONING, MOLECULAR; CYTOPLASM; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEK293 CELLS; HELA CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PATCH-CLAMP TECHNIQUES; PHORBOLS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN STRUCTURE, TERTIARY; TRPV CATION CHANNELS;

EID: 84878677214     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1220231110     Document Type: Article

References (51)

1. Strotmann R, Harteneck C, Nunnenmacher K, Schultz G, Plant TD (2000) OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol 2(10):695-702.
2. Liedtke W, et al. (2000) Vanilloid receptor-related osmotically activated channel (VROAC), a candidate vertebrate osmoreceptor. Cell 103(3):525-535.
3. Wissenbach U, Bödding M, Freichel M, Flockerzi V (2000) Trp12, a novel Trp related protein from kidney. FEBS Lett 485(2-3):127-134.
4. Arniges M, Vázquez E, Fernández-Fernández JM, Valverde MA (2004) Swelling-activated Ca2+ entry via TRPV4 channel is defective in cystic fibrosis airway epithelia. J Biol Chem 279(52):54062-54068.
5. Suzuki M, Mizuno A, Kodaira K, Imai M (2003) Impaired pressure sensation in mice lacking TRPV4. J Biol Chem 278(25):22664-22668.
6. Liedtke W, Tobin DM, Bargmann CI, Friedman JM (2003) Mammalian TRPV4 (VR-OAC) directs behavioral responses to osmotic and mechanical stimuli in Caenorhabditis elegans. Proc Natl Acad Sci USA 100(Suppl 2):14531-14536.
7. Andrade YN, et al. (2005) TRPV4 channel is involved in the coupling of fluid viscosity changes to epithelial ciliary activity. J Cell Biol 168(6):869-874.
8. Güler AD, et al. (2002) Heat-evoked activation of the ion channel, TRPV4. J Neurosci 22(15):6408-6414.
9. Fernández-Fernández JM, et al. (2008) Functional coupling of TRPV4 cationic channel and large conductance, calcium-dependent potassium channel in human bronchial epithelial cell lines. Pflugers Arch 457(1):149-159.
10. Liedtke W, Friedman JM (2003) Abnormal osmotic regulation in trpv4-/- mice. Proc Natl Acad Sci USA 100(23):13698-13703.
11. Vriens J, et al. (2005) Modulation of the Ca2-permeable cation channel TRPV4 by cytochrome P450 epoxygenases in vascular endothelium. Circ Res 97(9):908-915.
12. Earley S, Heppner TJ, Nelson MT, Brayden JE (2005) TRPV4 forms a novel Ca2+ signaling complex with ryanodine receptors and BKCa channels. Circ Res 97(12):1270-1279.
13. Alessandri-Haber N, Dina OA, Joseph EK, Reichling D, Levine JD (2006) A transient receptor potential vanilloid 4-dependent mechanism of hyperalgesia is engaged by concerted action of inflammatory mediators. J Neurosci 26(14):3864-3874.
14. Cohen DM (2005) TRPV4 and the mammalian kidney. Pflugers Arch 451(1):168-175.
15. Gevaert T, et al. (2007) Deletion of the transient receptor potential cation channel TRPV4 impairs murine bladder voiding. J Clin Invest 117(11):3453-3462.
16. Fernandes J, et al. (2008) IP3 sensitizes TRPV4 channel to the mechano- and osmotransducing messenger 5'-6'-epoxyeicosatrienoic acid. J Cell Biol 181(1):143-155.
17. Lorenzo IM, Liedtke W, Sanderson MJ, Valverde MA (2008) TRPV4 channel participates in receptor-operated calcium entry and ciliary beat frequency regulation in mouse airway epithelial cells. Proc Natl Acad Sci USA 105(34):12611-12616.
18. Muramatsu S, et al. (2007) Functional gene screening system identified TRPV4 as a regulator of chondrogenic differentiation. J Biol Chem 282(44):32158-32167.
19. Masuyama R, et al. (2008) TRPV4-mediated calcium influx regulates terminal differentiation of osteoclasts. Cell Metab 8(3):257-265.
20. Vriens J, et al. (2004) Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc Natl Acad Sci USA 101(1):396-401.
21. Watanabe H, et al. (2002) Heat-evoked activation of TRPV4 channels in a HEK293 cell expression system and in native mouse aorta endothelial cells. J Biol Chem 277(49): 47044-47051.
22. Loukin S, Zhou X, Su Z, Saimi Y, Kung C (2010) Wild-type and brachyolmia-causing mutant TRPV4 channels respond directly to stretch force. J Biol Chem 285(35): 27176-27181.
23. Strotmann R, Schultz G, Plant TD (2003) Ca2+-dependent potentiation of the nonselective cation channel TRPV4 is mediated by a C-terminal calmodulin binding site. J Biol Chem 278(29):26541-26549.
24. Phelps CB, Wang RR, Choo SS, Gaudet R (2010) Differential regulation of TRPV1, TRPV3, and TRPV4 sensitivity through a conserved binding site on the ankyrin repeat domain. J Biol Chem 285(1):731-740.
25. D'hoedt D, et al. (2008) Stimulus-specific modulation of the cation channel TRPV4 by PACSIN 3. J Biol Chem 283(10):6272-6280.
26. Garcia-Elias A, Lorenzo IM, Vicente R, Valverde MA (2008) IP3 receptor binds to and sensitizes TRPV4 channel to osmotic stimuli via a calmodulin-binding site. J Biol Chem 283(46):31284-31288.
27. Vriens J, Owsianik G, Janssens A, Voets T, Nilius B (2007) Determinants of 4 alphaphorbol sensitivity in transmembrane domains 3 and 4 of the cation channel TRPV4. J Biol Chem 282(17):12796-12803.
28. Verma P, Kumar A, Goswami C (2010) TRPV4-mediated channelopathies. Channels (Austin) 4(4):319-328.
29. Nilius B, Owsianik G, Voets T (2008) Transient receptor potential channels meet phosphoinositides. EMBO J 27(21):2809-2816.
30. Rohacs T (2009) Phosphoinositide regulation of non-canonical transient receptor potential channels. Cell Calcium 45(6):554-565.
31. Prescott ED, Julius D (2003) A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science 300(5623):1284-1288.
32. Brauchi S, et al. (2007) Dissection of the components for PIP2 activation and thermosensation in TRP channels. Proc Natl Acad Sci USA 104(24):10246-10251.
33. Nilius B, et al. (2006) The Ca2+-activated cation channel TRPM4 is regulated by phosphatidylinositol 4,5-biphosphate. EMBO J 25(3):467-478.
34. Lukacs V, et al. (2007) Dual regulation of TRPV1 by phosphoinositides. J Neurosci 27(26):7070-7080.
35. Hansen SB, Tao X, MacKinnon R (2011) Structural basis of PIP2 activation of the classical inward rectifier K+ channel Kir2.2. Nature 477(7365):495-498.
36. Whorton MR, MacKinnon R (2011) Crystal structure of the mammalian GIRK2 K+ channel and gating regulation by G proteins, PIP2, and sodium. Cell 147(1):199-208.
37. Tian W, et al. (2009) A loss-of-function nonsynonymous polymorphism in the osmoregulatory TRPV4 gene is associated with human hyponatremia. Proc Natl Acad Sci USA 106(33):14034-14039.
38. Gamper N, Rohacs T (2012) Phosphoinositide sensitivity of ion channels, a functional perspective. Subcell Biochem 59:289-333.
39. Suh BC, Inoue T, Meyer T, Hille B (2006) Rapid chemically induced changes of PtdIns (4,5)P2 gate KCNQ ion channels. Science 314(5804):1454-1457.
40. Rohács T, Lopes CM, Michailidis I, Logothetis DE (2005) PI(4,5)P2 regulates the activation and desensitization of TRPM8 channels through the TRP domain. Nat Neurosci 8(5):626-634.
41. Watanabe H, et al. (2003) Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature 424(6947):434-438.
42. Everaerts W, et al. (2010) Inhibition of the cation channel TRPV4 improves bladder function in mice and rats with cyclophosphamide-induced cystitis. Proc Natl Acad Sci USA 107(44):19084-19089.
43. Chung MK, Lee H, Caterina MJ (2003) Warm temperatures activate TRPV4 in mouse 308 keratinocytes. J Biol Chem 278(34):32037-32046.
44. Cuajungco MP, et al. (2006) PACSINs bind to the TRPV4 cation channel: PACSIN 3 modulates the subcellular localization of TRPV4. J Biol Chem 281(27):18753-18762.
45. Wang Q, et al. (2009) Molecular mechanism of membrane constriction and tubulation mediated by the F-BAR protein Pacsin/Syndapin. Proc Natl Acad Sci USA 106(31): 12700-12705.
46. Plomann M, Wittmann JG, Rudolph MG (2010) A hinge in the distal end of the PACSIN 2 F-BAR domain may contribute to membrane-curvature sensing. JMol Biol 400(2):129-136.
47. Plomann M, Mörgelin M, Schael S (2009) The PACSIN proteins and their role in mebrane trafficking. The Pombe Cdc15 Homology Proteins, ed Aspenström P (Landes Biosciences, Austin, TX), pp 39-48.
48. Arniges M, Fernández-Fernández JM, Albrecht N, Schaefer M, Valverde MA (2006) Human TRPV4 channel splice variants revealed a key role of ankyrin domains in multimerization and trafficking. J Biol Chem 281(3):1580-1586.
49. Cao E, Cordero-Morales JF, Liu B, Qin F, Julius D (2013) TRPV1 channels are intrinsically heat-sensitive and negatively regulated by phosphoinositide lipids. Neuron 77(4):667-679.
50. Jin X, Touhey J, Gaudet R (2006) Structure of the N-terminal ankyrin repeat domain of the TRPV2 ion channel. J Biol Chem 281(35):25006-25010.
51. Inada H, Procko E, Sotomayor M, Gaudet R (2012) Structural and biochemical consequences of disease-causing mutations in the ankyrin repeat domain of the human TRPV4 channel. Biochemistry 51(31):6195-6206.