Glycosylation of the osmoresponsive transient receptor potential channel TRPV4 on Asn-651 influences membrane trafficking

American Journal of Physiology - Renal Physiology

Volumn 290, Issue 5, 2006, Pages

  Xu, Hongshi ^a,b   Fu, Yi ^a,b   Tian, Wei ^a,b   Cohen, David M ^a,b,c  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b PORTLAND VA MEDICAL CENTER   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Cell volume regulation; Hypotonicity; Ion channel

Indexed keywords

ASPARAGINE; CALCIUM; GLUTAMINE; LECTIN; POTASSIUM CHANNEL HERG; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL VANILLOID 4; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL CELL; ARTICLE; CELL LYSATE; CELL MEMBRANE; CONTROLLED STUDY; GLYCOSYLATION; HUMAN; HUMAN CELL; HYPERPOLARIZATION; IMMUNOBLOTTING; IMMUNOREACTIVITY; MEMBRANE POTENTIAL; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN STRUCTURE;

EID: 33646542001     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00245.2005     Document Type: Article

References (57)

1. 2+ entry via TRPV4 channel is defective in cystic fibrosis airway epithelia. J Biol Chem 279: 54062-54068, 2004.
2. Barnhill JC, Stokes AJ, Koblan-Huberson M, Shimoda LM, Muraguchi A, Adra CN, and Turner H. RGA protein associates with a TRPV ion channel during biosynthesis and trafficking. J Cell Biochem 91: 808-820, 2004.
3. Becker D, Blase C, Bereiter-Hahn J, and Jendrach M. TRPV4 exhibits a functional role in cell-volume regulation. J Cell Sci 118: 2435-2440, 2005.
4. Bennett E, Urcan MS, Tinkle SS, Koszowski AG, and Levinson SR. Contribution of sialic acid to the voltage dependence of sodium channel gating. A possible electrostatic mechanism. J Gen Physiol 109: 327-343, 1997.
5. Bezzerides VJ, Ramsey IS, Kotecha S, Greka A, and Clapham DE. Rapid vesicular translocation and insertion of TRP channels. Nat Cell Biol 6: 709-720, 2004.
6. Blom N, Sicheritz-Ponten T, Gupta R, Gammeltoft S, and Brunak S. Prediction of posttranslational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4: 1633-1649, 2004.
7. Cayouette S, Lussier MP, Mathieu EL, Bousquet SM, and Boulay G. Exocytotic insertion of TRPC6 channel into the plasma membrane upon Gq protein-coupled receptor activation. J Biol Chem 279: 7241-7246, 2004.
8. Chang Q, Hoefs S, van der Kemp AW, Topala CN, Bindels RJ, and Hoenderop JG. The β-glucuronidase klotho hydrolyzes and activates the TRPV5 channel. Science 310: 490-493, 2005.
9. Clapham DE. TRP channels as cellular sensors. Nature 426: 517-524, 2003.
10. Cronin NB, O'Reilly A, Duclohier H, and Wallace BA. Effects of deglycosylation of sodium channels on their structure and function. Biochemistry 44: 441-449, 2005.
11. Cserzo M, Wallin E, Simon I, von Heijne G, and Elofsson A. Prediction of transmembrane α-helices in prokaryotic membrane proteins: the dense alignment surface method. Protein Eng 10: 673-676, 1997.
12. De Souza NF and Simon SM. Glycosylation affects the rate of traffic of the Shaker potassium channel through the secretory pathway. Biochemistry 41: 11351-11361, 2002.
13. Delany NS, Hurle M, Facer P, Alnadaf T, Plumpton C, Kinghorn I, See CG, Costigan M, Anand P, Woolf CJ, Crowther D, Sanseau P, and Tate SN. Identification and characterization of a novel human vanilloid receptor-like protein, VRL-2. Physiol Genomics 4: 165-174, 2001.
14. Dietrich A, Mederos y Schnitzler M, Emmel J, Kalwa H, Hofmann T, and Gudermann T. N-linked protein glycosylation is a major determinant for basal TRPC3 and TRPC6 channel activity. J Biol Chem 278: 47842-47852, 2003.
15. 2+ channel TRPV5 by the NHE regulating factor NHERF2 and the serum and glucocorticoid inducible kinase isoforms SGK1 and SGK3 expressed in Xenopus oocytes. Cell Physiol Biochem 14: 203-212, 2004.
16. Fozzard HA and Kyle JW. Do defects in ion channel glycosylation set the stage for lethal cardiac arrhythmias? Sci STKE 2002: PE19, 2002.
17. Freeman LC, Lippold JJ, and Mitchell KE. Glycosylation influences gating and pH sensitivity of I(sK). J Membr Biol 177: 65-79, 2000.
18. Gong Q, Anderson CL, January CT, and Zhou Z. Role of glycosylation in cell surface expression and stability of HERG potassium channels. Am J Physiol Heart Circ Physiol 283: H77-H84, 2002.
19. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450, 1985.
20. Jia Y, Wang X, Varty L, Rizzo CA, Yang R, Correll CC, Phelps PT, Egan RW, and Hey JA. Functional TRPV4 channels are expressed in human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 287: L272-L278, 2004.
21. Kanzaki M, Zhang YQ, Mashima H, Li L, Shibata H, and Kojima I. Translocation of a calcium-permeable cation channel induced by insulin-like growth factor-I. Nat Cell Biol 1: 165-170, 1999.
22. Khanna R, Myers MP, Laine M, and Papazian DM. Glycosylation increases potassium channel stability and surface expression in mammalian cells. J Biol Chem 276: 34028-34034, 2001.
23. Kuro-o M, Matsumura Y, Aizawa H, Kawaguchi H, Suga T, Utsugi T, Ohyama Y, Kurabayashi M, Kaname T, Kume E, Iwasaki H, Iida A, Shiraki-Iida T, Nishikawa S, Nagai R, and Nabeshima Y. Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature 390: 45-51, 1997.
24. Liedtke W, Choe Y, Marti-Renom MA, Bell AM, Denis CS, Sali A, Hudspeth AJ, Friedman JM, and Heller S. Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103: 525-535, 2000.
25. Liedtke W and Friedman JM. Abnormal osmotic regulation in trpv4-/- mice. Proc Natl Acad Sci USA 100: 13698-13703, 2003.
26. Lodish HF, Berk A, Zipursky SL, Matsudaira P, Baltimore D, and Darnell JE Jr. Protein sorting: organelle biogenesis and protein secretion. In: Molecular Cell Biology. New York: W. H. Freeman, 1999, p. 712-722.
27. Mery L, Strauss B, Dufour JF, Krause KH, and Hoth M. The PDZ-interacting domain of TRPC4 controls its localization and surface expression in HEK293 cells. J Cell Sci 115: 3497-3508, 2002.
28. Mizuno A, Matsumoto N, Imai M, and Suzuki M. Impaired osmotic sensation in mice lacking TRPV4. Am J Physiol Cell Physiol 285: C96-C101, 2003.
29. Morenilla-Palao C, Planells-Cases R, Garcia-Sanz N, and Ferrer-Montiel A. Regulated exocytosis contributes to protein kinase C potentiation of vanilloid receptor activity. J Biol Chem 279: 25665-25672, 2004.
30. Much B, Wahl-Schott C, Zong X, Schneider A, Baumann L, Moosmang S, Ludwig A, and Biel M. Role of subunit heteromerization and N-linked glycosylation in the formation of functional hyperpolarization-activated cyclic nucleotide-gated channels. J Biol Chem 278: 43781-43786, 2003.
31. Pabon A, Chan KW, Sui JL, Wu X, Logothetis DE, and Thornhill WB. Glycosylation of GIRK1 at Asn119 and ROMK1 at Asn117 has different consequences in potassium channel function. J Biol Chem 275: 30677-30682, 2000.
32. 2+ channel TRPV5 by the NHE regulating factor NHERF2 and the serum and glucocorticoid inducible kinase SGK1. Cell Physiol Biochem 15: 175-182, 2005.
33. Petrecca K, Atanasiu R, Akhavan A, and Shrier A. N-linked glycosylation sites determine HERG channel surface membrane expression. J Physiol 515: 41-48, 1999.
34. Recio-Pinto E, Thornhill WB, Duch DS, Levinson SR, and Urban BW. Neuraminidase treatment modifies the function of electroplax sodium channels in planar lipid bilayers. Neuron 5: 675-684, 1990.
35. 2+ channels in vascular smooth muscle cells. J Biol Chem 272: 32240-32246, 1997.
36. Santacruz-Toloza L, Huang Y, John SA, and Papazian DM. Glycosylation of shaker potassium channel protein in insect cell culture and in Xenopus oocytes. Biochemistry 33: 5607-5613, 1994.
37. Satler CA, Vesely MR, Duggal P, Ginsburg GS, and Beggs AH. Multiple different missense mutations in the pore region of HERG in patients with long QT syndrome. Hum Genet 102: 265-272, 1998.
38. + channels in mammalian brain and in transfected cells. J Membr Biol 168: 265-273, 1999.
39. 2+ influx. Mol Cell 15: 635-646, 2004.
40. Stokes AJ, Shimoda LM, Koblan-Huberson M, Adra CN, and Turner H. A TRPV2-PKA signaling module for transduction of physical stimuli in mast cells. J Exp Med 200: 137-147, 2004.
41. Stokes AJ, Wakano C, Del Carmen KA, Koblan-Huberson M, and Turner H. Formation of a physiological complex between TRPV2 and RGA protein promotes cell surface expression of TRPV2. J Cell Biochem 94: 669-683, 2005.
42. Strotmann R, Harteneck C, Nunnenmacher K, Schultz G, and Plant TD. OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol 2: 695-702, 2000.
43. Thornhill WB, Wu MB, Jiang X, Wu X, Morgan PT, and Margiotta JF. Expression of Kv1.1 delayed rectifier potassium channels in Lec mutant Chinese hamster ovary cell lines reveals a role for sialidation in channel function. J Biol Chem 271: 19093-19098, 1996.
44. Traub O, Monia BP, Dean NM, and Berk BC. PKC- is required for mechano-sensitive activation of ERK1/2 in endothelial cells. J Biol Chem 272: 31251-31257, 1997.
45. Tyrrell L, Renganathan M, Dib-Hajj SD, and Waxman SG. Glycosylation alters steady-state inactivation of sodium channel Nav1.9/NaN in dorsal root ganglion neurons and is developmentally regulated. J Neurosci 21: 9629-9637, 2001.
46. Ufret-Vincenty CA, Baro DJ, Lederer WJ, Rockman HA, Quinones LE, and Santana LF. Role of sodium channel deglycosylation in the genesis of cardiac arrhythmias in heart failure. J Biol Chem 276: 28197-28203, 2001.
47. + currents in ventricular myocytes. Am J Physiol Cell Physiol 281: C464-C474, 2001.
48. Vannier B, Zhu X, Brown D, and Birnbaumer L. The membrane topology of human transient receptor potential 3 as inferred from glycosylation-scanning mutagenesis and epitope immunocytochemistry. J Biol Chem 273: 8675-8679, 1998.
49. Vriens J, Watanabe H, Janssens A, Droogmans G, Voets T, and Nilius B. Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc Natl Acad Sci USA 101: 396-401, 2004.
50. Watanabe H, Vriens J, Prenen J, Droogmans G, Voets T, and Nilius B. Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature 424: 434-438, 2003.
51. Watanabe I, Wang HG, Sutachan JJ, Zhu J, Recio-Pinto E, and Thornhill WB. Glycosylation affects rat Kv1.1 potassium channel gating by a combined surface potential and cooperative subunit interaction mechanism. J Physiol 550: 51-66, 2003.
52. Watanabe I, Zhu J, Recio-Pinto E, and Thornhill WB. Glycosylation affects the protein stability and cell surface expression of Kv1.4 but not Kv11 potassium channels. A pore region determinant dictates the effect of glycosylation on trafficking. J Biol Chem 279: 8879-8885, 2004.
53. Wissenbach U, Bodding M, Freichel M, and Flockerzi V. Trp12, a novel Trp related protein from kidney. FEBS Lett 485: 127-134, 2000.
54. Xu H, Zhao H, Tian W, Yoshida K, Roullet JB, and Cohen DM. Regulation of a transient receptor potential (TRP) channel by tyrosine phosphorylation. SRC family kinase-dependent tyrosine phosphorylation of TRPV4 on TYR-253 mediates its response to hypotonic stress. J Biol Chem 278: 11520-11527, 2003.
55. Yu FH and Catterall WA. The VGL-chanome: a protein superfamily specialized for electrical signaling and ionic homeostasis. Sci STKE 2004: re15, 2004.
56. Zhang Y, Hartmann HA, and Satin J. Glycosylation influences voltage-dependent gating of cardiac and skeletal muscle sodium channels. J Membr Biol 171: 195-207, 1999.
57. Zhu J, Watanabe I, Poholek A, Koss M, Gomez B, Yan C, Recio-Pinto E, and Thornhill WB. Allowed N-glycosylation sites on the Kv1.2 potassium channel S1-S2 linker: implications for linker secondary structure and the glycosylation effect on channel function. Biochem J 375: 769-775, 2003.