Understanding ion channel biology using epitope tags: Progress, pitfalls, and promise

Journal of Cellular Physiology

Volumn 213, Issue 3, 2007, Pages 618-625

  Maue, Robert A ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ALPHA BUNGAROTOXIN; C PEPTIDE; CHLORIDE CHANNEL; CHOLINERGIC RECEPTOR; CYAN FLUORESCENT PROTEIN; EPITOPE; GLUTAMATE RECEPTOR; GLYCINE RECEPTOR; GLYCOPROTEIN D; GREEN FLUORESCENT PROTEIN; HEMAGGLUTININ; ION CHANNEL; MUCIN; MYC PROTEIN; POTASSIUM CHANNEL; PURINE RECEPTOR; SEROTONIN RECEPTOR; STREPTAVIDIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSMEMBRANE CONDUCTANCE REGULATOR; VIRUS T ANTIGEN; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL; YELLOW FLUORESCENT PROTEIN;

CELLULAR DISTRIBUTION; CHANNEL GATING; ENDOCYTOSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; ONCOGENE C MYC; ONCOGENE H RAS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; RECOMBINANT DNA TECHNOLOGY; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SHORT SURVEY; WESTERN BLOTTING;

ANIMALS; EPITOPE MAPPING; EPITOPES; FORECASTING; GREEN FLUORESCENT PROTEINS; HEMAGGLUTININS; HISTIDINE; HUMANS; IMMUNOHISTOCHEMISTRY; ION CHANNELS; PEPTIDES; PROTO-ONCOGENE PROTEINS C-MYC;

EID: 35848951177     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21259     Document Type: Short Survey

References (127)

1. Alldred MJ, Mulder-Rosi J, Lingenfelter SE, Chen G, Luscher B. 2005. Distinct γ2 subunit domains mediate clustering and synaptic function of postsynaptic GABAA receptors and gephryin. J Neurosci 25:594-603.
2. Anand R, Bason L, Saedi MS, Gerzanich V, Peng X, Lindstrom J. 1993. Reporter epitopes: A novel approach to determine transmembrane topology of integral membrane proteins applied to the α1 subunit of the nicotinic acetylcholine receptor. Biochemistry 32:9975-9984.
3. Andoo R, Mizuno H, Miyawaki A. 2004. Regulated fast nucleocytoplasmic shuttling obsevred by reversible protein highlighting. Science 306:1370-1373.
4. Antonucci DE, Lim ST, Vassanelli S, Trimmer JS. 2001. Dynamic localization and clustering of dendritic Kv2.1 voltage-dependent potassium channels in developing hippocampal neurons. Neuroscience 108:69-81.
5. Ashby MC, De La Rue SA, Ralph GS, Uney J, Collinridge GL, Henley JM. 2004a. Removal of AMPA receptors (AMPARs) from synapses is preceded by transient endocytosis of extrasynaptic AMPARs. J Neurosci 24:5172-5178.
6. Ashby MC, Ibaraki K, Henley JM. 2004b. Its green outside: Tracking cell surface proteins with pH-sensitive GFP. Trends Neurosci 27:257-261.
7. Backman CM, Zhang Y, Hoffer BJ, Tomac AC. 2004. Tetracycline-inducible expression systems for the generation of transgenic animals: A comparison of various inducible systems carried in a single vector. J Neurosci Meth 139:257-262.
8. 3 receptors. Proc Natl Acad Sci 102:12595-12600.
9. 2/6 receptor heteromers depends on relative subunit expression levels. Biophys J 93:505-512.
10. Beitz E, Liu K, Ikeda M, Guggino WB, Agre P, Yasui M. 2006. Determinants of AQP6 trafficking to intracellular sites versus the plasma memrane in transfected mammalian cells. Biol Cell 98:101-109.
11. + channel subunits measured with a confocal microscope and a streak camera. Nature Biotechnol 22:220-224.
12. Brothers SP, Janovik JA, Conn PM. 2003. Unexpected effects of epitope and chimeric tags on gonadotropin-releasing hormone receptors: Implications for understanding the molecular etiology of hypogonadotropic hypogonadism. J Clin Endocrinol Metabol 88:6107-6112.
13. A receptor-GFP chimera expressed in Xenopus oocytes. Mol Brain Res 59:165-177.
14. Bukauskas F, Jordan K, Bukauskiene A, Bennett MVL, Lampe PD, Laird DW, Verselis VK. 2000. Clustering of connexin 43-enhanced green fluorescent protein gap junction channels and functional coupling in living cells. Proc Natl Acad Sci 97:2556-2561.
15. Cai J, Yi F-F, Li Y-H, Yang X-C, Song J, Jiang X-J, Jiang H, Lin G-S, Wan W. 2007. Adenoviral gene transfer of HCN4 creates a genetic pacemaker in pigs with complete atrioventricular block. Life Sci 80:1746-1753.
16. Chai S, Li M, Lan JQ, Xiong Z-G, Saugstad JA, Simon RP. 2007. A kinase-anchoring protein 150 and calcineurin are involved in regulation of acid-sensing ion channels ASIC1a and ASIC2a. J Biol Chem 282:22668-22677.
17. Chen J, Micheson JS, Lin M, Sanguinetti MC. 2000. Functional roles of charged residues in the putative voltage sensor of the HCN2 pacemaker channel. J Biol Chem 275:36465-36471.
18. Chen YG, Maika SD, Stevens SW. 2006. Epitope tagging of proteins at the native chromosomal loci of genes in mice and in cultured vertebrate cells. J Mol Biol 361:412-419.
19. +2 channels. J Biol Chem 270:30036-30044.
20. +2 channel β subunits revealed by their expression in adult rat heart cells. J Physiol 541:435-452.
21. A receptor α1 subunit tagged with green fluorescent protein requires a a β subunit for functional surface expression. J Biol Chem 273:28906-28911.
22. Cooper ST, Millar NS. 1997. Host cell-specific folding and assembly of the neuronal nicotininc acetylcholine receptor α7 subunit. J Neurochem 68:2140-2151.
23. Crusius K, Finster S, McClary J, Xia W, Larson B, Schneider D, Lu H-T, Biancalana S, Xuan J, Newton A, Allen D, Bringmann P, Cobb RR. 2006. Tab2, a novel recombinant polypeptide tag offering sensitive and specific protein detection and reliable affinity purification. Gene 380:111-119.
24. Delling M, Wischmeyer E, Dityatev A, Sytnyk V, Veh RW, Karschin A, Schachner M. 2002. The neural cell adhesion molecule regulates cell-surface delivery of G-protein-activated inwardly rectifying potassium channels via lipid rafts. J Neurosci 22:7154-7164.
25. Dubel SJ, Altier C, Chaumont S, Lory P, Bourinet E, Nargeot J. 2004. Plasma membrane expression of T-type calcium channel α1 subunits is modulated by high voltage-ativated auxiliary subunits. J Biol Chem 279:29263-29269.
26. Evans GI, Lewis GK, Ramsey G, Bishop JM. 1985. Isolation of monoclonal antibodies specific for human c-myc proto oncogene product. Mol Cell Biol 5:3610-3616.
27. Field J, Nikawa JI, Broek D, MacDonald B, Rodgers L, Wilson IA, Lerner RA, Wigler M. 1988. Purification of a ras-responsive adenylyl cyclase complex from yeast by use of an epitope addition method. Mol Cell Biol 8:2159-2165.
28. + channel β1 subunits tagged with a yellow fluorescent protein. J Neurosci Res 74:794-800.
29. Fucile S, Palma E, Martinez-Torres A, Mildei R, Eusebi F. 2002. The single-channel properties of human acetylcholine α7 receptors are altered by fusing α7 to the green fluorescent protein. Proc Natl Acad Sci 99:3956-3961.
30. Gao Y, Liu S-S, Qiu S, Cheng W, Zheng J, Luo J-H. 2007. Fluorescence resonance energy transfer analysis of subunit assembly of the ASIC channel. Biochem Biophys Res Commun 359:143-150.
31. Gensler S, Sander A, Korngreen A, Traina G, Giese G, Witzmann V. 2001. Assembly and clustering of acetylcholine receptors containing GFP-tagged epsilon or gamma subunits: selective targeting to the neuromuscular junction in vivo. Eur J Biochem 268:2209-2217.
32. Giraldez T, Hughes TE, Sigworth FJ. 2005. Generation of functional fluorescent BK channels by random insertion of GFP variants. J Gen Physiol 126:429-438.
33. Giraldez T, Afonso-Oramas D, Cruz-Muros I, Garcia-Martin V, Pagel P, Gonzalez-Hernandez T, Alvarez de la Rosa D. 2007. Cloning and functional expression of a new epithelial sodium channel δ subunit isoform differentially expressed in neurons of the human and monkey telencephalon. J Neuorchem 102:1304-1315.
34. Grussenmeyer T, Scheidtmann KH, Hutchinson MA, Eckhart W, Walter G. 1985. Complexes of polyoma virus medium T antigen and cellular proteins. Proc Natl Acad Sci 82:7952-7954.
35. Gu C, Jan YN, Jan LY. 2003. A conserved domain in axonal targeting of Kv1 voltage-gated potassium channels. Science 301:646-649.
36. Hackbarth JS, Lee S-H, Meng XW, Vroman BT, Kaufmann SH, Karnitz LM. 2004. S-peptide epitope tagging for protein purification, expression monitoring, and localization in mammalian cells. Biotechniques 37:835-839.
37. + channel expressed in epithelial Madin-Darby canine kidney cells. J Biol Chem 277:9772-9779.
38. Hellwig N, Albrecht N, Hartenneck C, Schultz G, Schaefer M. 2005. Homo- and heteromeric assembly of TRPV channel subunits. J Cell Sci 118:917-928.
39. Hopp TP, Prickett KS, Price VL, Libby RT, March CJ, Ceretti DP, Urdal DL, Conlon PJ. 1988. A short polypeptide marker sequence useful for recombinant protein identification and purification. Biotechnology 6:1204-1210.
40. Hoque ATMS, Liu X, Kagami H, Swain WD, Wellner RB, O'Connell BC, Ambudkar IS, Baum BJ. 2000. Construction and function of a recombinant adenovirus encoding a human aquaporin 1-green fluorescent protein fusion product. Cancer Gene Ther 7:476-485.
41. Houle TD, Ram ML, McMurray WJ, Cala SE. 2006. Different endoplasmic reticulum trafficking and processing pathways for calsequestrin (CSQ) and epitope-tagged CSQ. Exp Cell Res 312:4150-4161.
42. + channel involves proteolytic processing of the α and γ- subunits. J Biol Chem 278:37073-37082.
43. A receptors. J Neurosci 25:10469-10478.
44. Jerome KR, Barnd DL, Bendt DM, Boyer CM, Taylor-Papadimitriou J, McKenzie IFC, Bast RC, Finn OJ. 1991. Cytotoxic T-lymphocytes derived from patients with breast adenocarcinoma recognize an epitope present on the protein core of a mucin molecule preferentially expressed by malignant cells. Cancer Res 51:2908-2916.
45. + channels linked to the green fluorescent protein in human embryonic kidney cells (HEK 293). J Physiol 510:333-345.
46. Johnson KY, Liu LY, Vincent TS. 2002. Minimal FLAG sequence useful in the functional epitope tagging of H-ras. Biotechniques 32:1270-1280.
47. Kato M, Ogura K, Miake J, Sasaki N, Taniguchi S, Igawa O, Yoshida A, Hoshikawa Y, Murata M, Nanba E, Kurata Y, Kawata Y, Ninomiya H, Morisaki T, Kitakaze M, Hisatome I. 2005. Evidence for proteasomal degredation of Kv1.5 channel protein. Biochem Biophys Res Commun 337:343-348.
48. Kearney JA, Plummer NW, Smith MR, Kapur J, Cummins TR, Waxman SG, Goldin AL, Meisler MH. 2001. A gain-of-function mutation in the sodium channel gene SCN2a results in seizures and behavioral abnormalities. Neuroscience 102:307-317.
49. Kennedy ME, Nemec J, Corey S, Wickman K, Clapham DE. 1999. GIRK4 confers appropriate processingand cell surface localization to G-p rote in-gated potassium channels. J Biol Chem 274:2571-2582.
50. 2 and α4β2 nicotinic channels measured with fluorescence resonance energy transfer and total internal reflection fluorescence microscopy. J Neurosci 25:6911-6920.
51. A receptor assembly in mammalian cell lines and hippocamapal neurons using γ2 subunit green fluorescent protein chimeras. Mol Cell Neurosci 16:440-452.
52. Kolodziej PA, Young RA. 1991. Epitope tagging and protein surveillance. Methods Enzymol 194:508-519.
53. Kosugi-Tanaka C, Li X, Yao C, Akamatsu T, Kanamori N, Hosoi K. 2006. Protein kinase A-regulated membrane trafficking of a green fluorescent protein-aquaporin 5 chimera in MDCK cells. Biochemicia et Biphysica Acta 1763:337-344.
54. Kraner SD, Fliatov GN, Sun W, Bannerman P, Lindstrom J, Barchi RL. 1998. Analysis of local structure in the D2/S1 region of the rat skeletal muscle type I sodium channel using insertional mutagenesis. J Neurochem 70:1628-1635.
55. Kreis TE, Lodish HF. 1986. Oligomerzation is essential for transport of vesicular stomatitis viral glycoprotein to the cell surface. Cell 46:929-937.
56. Kupper J. 1998. Functional expression of GFP-tagged Kv1.3 and Kv1.4 channels in HEK 293 cells. Eur J Neurosci 10:3908-3912.
57. Lavezzari G, McCallum J, Dewey CM, Roche KW. 2004. Subunit specific regulation of NMDA receptor endocytosis. J Neurosci 24:6383-6391.
58. + channel in Aplysia neuron R15. Neurosci Lett 349:53-57.
59. Lee SH, Simonetta A, Sheng M. 2004. Subunit rules governing the sorting of internalized AMPA receptors in hippocampal neurons. Neuron 43:221-235.
60. Leroy J, Richards MS, Butcher AJ, Nieto-Rostro M, Prsatt WS, Davies A, Dolphin AC. 2005. Interaction via key tryptophan in the I-II linker of N-type calcium channels is required for β1 but not for palmitoylated β2, implicating an additional binding site in the regulation of channel voltage-dependent properties. J Neurosci 25:6984-6996.
61. Li H, Guo W, Xu H, Hood R, Benedict AT, Nerbonne JM. 2001. Functional expression of a GFP-tagged Kv1.5 α-subunit in mouse ventricle. Am J Physiol Heart Circ Physiol 281:H1955-. H1967.
62. Li Y, Gamper N, Shapiro MS. 2004. Single-channel analysis of KCNQ K channels reveals the mechanism of augmentation by a cysteine-modifying reagent. J Neurosci 24:5079-5090.
63. Lichty JJ, Malecki JL, Agnew HD, Michelson-Horowitz DJ, Tan S. 2005. Comparison of affinity tags for protein purification. Protein Expr Purif 41:98-105.
64. Ling S, Woronuk G, Sy L, Lev S, Braun AP. 2000. Enhanced activity of a large conductance, calcium-sensitive K channel in the presence of src tyrosine kinase. J Biol Chem 275:30683-30689.
65. Lutz-Freyermuth C, Query CC, Keene JD. 1990. Quantitative determination that one of two potential RNA-binding domains of the A protein component of the U1 small nuclear ribonucleoprotein complex binds with high affinity to stem loop II of U1 RNA. Proc Natl Acad Sci 87:6393-6397.
66. MacArthur H, Walter G. 1984. Monoclonal antibodies specific for the carboxy terminus of simian virus 40 large T antigen. J Virol 52:483-491.
67. Marshall J, Molloy R, Moss GWJ, Howe JR, Hughes TE. 1995. The jellyfish green fluorescent protein: A new tool for studying ion channel expression and function. Neuron 14:211-215.
68. Mattar PA, Holmes KD, Dekaban GA. 2003. An antisense construct reduces n-methyl-D-aspartate receptor 2A expression and receptor-mediated excitotoxcitiy as determined by a novel flow cytometric approach. J Neurosci Res 74:782-793.
69. Matz MV, Lukyanov KA, Lukyanov SA. 2002. Family of the green fluorescent protein: Journey to the end of the rainbow. BioEssays 24:953-959.
70. Maximov A, Bezprozvanny I. 2002. Synaptic targeting of N-type calcium channels in hippocampal neurons. J Neurosci 22:6939-6952.
71. McCann CM, Bareyre FM, Lichtman JW, Sanes JR. 2005. Peptide tags for labeling membrane proteins in live cells with multiple fluorophores. Biotechniques 38:945-952.
72. Meltzer RH, Kapoor N, Qadri YJ, Anderson SJ, Fuller CM, Benos DJ. 2007. Heteromeric assembly of acid sensitive ion channel and epithelial sodium channel subunits. J Biol Chem doi/10.1074/jbc.M703825200.
73. + channel is suppressed by N-terminal GFP tag. Eur J Neurosci 11:1105-1108.
74. Miyawaki A. 2002. Green fluorescent protein-like proteins in reef Anthoza animals. Cell Struct Funct 27:343-347.
75. Morita T, Tanimura A, Nezu A, Tojyo Y. 2002. Visualization of inositol 1.4. 5-trisphosphate receptor type III with green fluorescent protein in living cells. Cell Calcium 31:59-64.
76. Moyer BD, Loffing J, Schweibert EM, Loffing-Cueni D, Halpin PA, Karlson KH, Isamilov II, Guggino WB, Langford GM, Stanton BA. 1998. Membrane trafficking of the cystic fibrosis gene product, cystic fibrosis transmembrane conductance regulator, tagged with green fluorescent protein in Madin-Darby canine kidney cells. J Biol Chem 273:21759-21768.
77. Neuhuber B, Gerster U, Mitterdorfer J, Glossmann H, Flucher BE. 1998. Differential effects of Ca channel β1a and β2a subunits on complex formation with α1s and on current expression in ts201 cells. J Biol Chem 273:91110-91118.
78. +2 channel α1 (Cav1.2) to synaptic and extrasynaptic compartments in hippocampal neurons. Eur J Neurosci 19:2109-2122.
79. Patterson GH, Lippincott-Schwartz J. 2002. A photoactivatable GFP for selective photo labeling of proteins and cells. Science 297:1873-1877.
80. Peng C, Rich ED, Varnum MD. 2004. Subunit configuration of heteromeric cone cyclic nucleotide-gated channels. Neuron 42:401-410.
81. Petrecca K, Atanasiu R, Akhavan A, Shrier A. 1999. N-linked glycosylation sites determine HERG channel surface membrane expression. J Physiol 515:41-48.
82. Petrecca K, Miller DM, Shrier A. 2000. Localization and enhanced current density of the Kv4.2 potassium channel by interaction with the actin-binding protein filamin. J Neurosci 20:8736-8744.
83. Philipson LH, Malayev A, Kunetsova A, Chang C, Nelson DJ. 1993. Functional and biochemical characterization of the human potassium channel Kv1.5 with a transplanted carboxy-terminal epitope in stable mammalian cell lines. Biochem Biophys Acta 1153:111-121.
84. Philipson LH, Kuznetsov A, Toth PT, Murphy JF, Szabo G, Ma GH, Miller RJ. 1995. Functional expression of an epitope-tagged G protein -coupled K channel (GIRK1). J Biol Chem 270:14604-14610.
85. Pinheiro PS, Perrais D, Coussen F, Barhanin J, Bettler B, Mann JR, Malva JO, Heinemann SF, Mulle C. 2007. Proc Natl Acad Sci 104:12181-12186.
86. Poteser M, Graziani A, Rosker C, Eder P, derler I, Kahr H, Zhu MX, Romanin C, Groschner K. 2006. TRPC3 and TRPC4 associate to form a redox-sensitive cation channel. J Biol Chem 281:13588-13595.
87. Prasher DC, Eckenrode VK, Ward WW, Prendergast FG, Cormier MJ. 1992. Primary structure of the Aequoria victoria green fluorescent protein. Gene 111:229-233.
88. 6-tagged proteins. Life Sci News 11:18-20.
89. Ren Z, Riley NJ, Garcia EP, Sanders JM, swanson GT, Marshall J. 2003. Multiple trafficking signals regualte kainate receptor KA2 subunit surface expression. J Neurosci 23:6608-6616.
90. Rosenberg M, Meier J, Triller A, Vannier C. 2001. Dynamics of glycine receptor insertion in the neuronal plasma membrane. J Neurosci 21:5036-5044.
91. Santoro B, Wainger BJ, Siegelbaum SA. 2004. Regulation of HCN channel surface expression y a novel c-terminal protein-protein interaction. J Neurosci 24:10750-10762.
92. Sarac R, Hou P, Hurley KM, Hriciste D, Cohen NA, Nelson DJ. 2005. Mutation of critical GIRK subunit residues disrupts N- and C-termini association and channel function. J Neurosci 25:1836-1846.
93. + channel subunits co-assemble: A potential new contributor to inward rectifier current heterogeneity. J Physiol 544:337-349.
94. Schultz BD, Takahashi A, Liu C, Frizzell RA, Howard M. 1997. FLAG epitope positioned in an external loop preserves normal biophysical properties of CFTR. Am J Physiol 273:C2080-C2089.
95. Sekar RB, Periasamy A. 2003. Fluorescence resonance energy transfer (FRET) microscopy imaging of live cell protein localization. J Cell Biol 160:629-633.
96. Sheridan DL, Berlot CH, Robert A, Inglis FM, Jakobsdottir KB, Howe JR, Hughes TE. 2002. A new way to rapidly create functional, fluorescent fusion proteins: Random insertion of GFP with an in vitro transposition reaction. BMC Neurosci 3:7.
97. Sheridan DL, Robert A, Cho CH, Howe JR, Hughes TE. 2006. Regions of α-amino-5-methyl-3-hydroxy-4-isoxazole proprionic acid receptor subunits that are permissive for the insertion of green fluorescent protein. Neuroscience 141:837-849.
98. Shevtsova Z, Malik JMI, Michel U, Scholl U, Bahr M, Kugler S. 2006. Evaluation of epitope tags for protein detection after in vivo CNS gene transfer. Eur J Neurosci 23:1961-1969.
99. Shi S-H, Hayashi Y, Petraliam RS, Zaman SH, Wenthold RJ, Svoboda K, Malinow R. 1999. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284:1811-1816.
100. Southern JA, Young DF, Heany F, Baumgartner WK, Randall RE. 1991. Identification of an epitope on the P and V proteins of simian virus S that distinguishes between two isolates with different biological characteristics. J Gen Virol 72:1551-1557.
101. Surdej P, Jacobs-Lorena M. 1994. Strategy for epitope tagging the protein coding region of any gene. Biotechniques 17:560-565.
102. Suzuki T, Rai T, Hayama A, Sohara E, Suda S, Itoh T, Sasaki S, Uchida S. 2006. Intracellular localization of CIC chloride channels and their ability to form hetero-oligomers. J Cell Physiol 206:792-798.
103. Szabo Z, Obermair GJ, Cooper CB, Zamponi GW, Flucher BE. 2006. Role of the synprint site in presynaptic targeting of the calcium channel Cav2.2 in hippocampal neurons. Eur J Neurosci 24:709-718.
104. A receptor β subunits that mediate both homomeric and heteromeric receptor expression. J Neurosci 19:6360-6371.
105. Terskikh A, Fradov A, Ermakova G, Zaraisky A, Tan P, Kajava AV, Zhao X, Lukyanov S, Matz M, Kim S, Weissman I, Siebert P. 2000. Fluorescent timer: Protein that changes color with time. Science 290:1585-1588.
106. Tikku S, Epshtein Y, Collins H, Travis AJ, Rothblat G, Levitan I. 2007. Relationship between Kir2.1/Kir2.3 activity and their distributions between cholesterol-rich and cholesterol-poor membrane domains. Am J Physiol Cell Physiol 293:C440-C450.
107. Tsien RY. 1998. The green fluorescent protein. Annu Rev Biochem 67:509-544.
108. + channel subunits mediated by the transmembrane domains. J Biol Chem 271:5866-5870.
109. Umenishi F, Verbavatz J-M, Verkman AS. 2000. cAMP regulated membrane diffusion of a green fluorescent protein-aquaporin 2 chimera. Biophys J 78:1024-1035.
110. Vais H, Gao G-P, Yang M, Tran P, Louboutin J-P, Somanathan S, Wilson JM, Reenstra WW. 2004. Novel adenovrial vectors coding for GFP-tagged wtCFTR and d508-CFTR: characterization of expression and electrophysiological properties in A549 cells. Pflugers Arch Eur J Physiol 449:278-287.
111. Wang Q, Liu L, Pei L, Ju W, Ahmadian G, Lu J, Wnag Y, Liu F, Wang YT. 2003. Control of synaptic strength, a novel function of Akt. Neuron 38:915-928.
112. Williams BM, Temburni MK, Levey MS, Bertrand S, Bertrand D, Jacob MH. 1998. The long internal loop of the α3 subunit targets nAChRs to subdomains within individual synapses on neurons in vivo. Nat Neurosci 1:557-562.
113. Wilson IA, Niman HL, Houghten RA, Cherensen AR, Connolly ML, Lemer RA. 1984. The structure of an antigenic determinant in a protein. Cell 37:77-778.
114. Wittemann S, Mark MD, Rettig J, Herlitze S. 2000. Synaptic localization and presynaptic function of calcium channel b4-subunits in cultured hippocampal neurons. J Biol Chem 275:37807-37814.
115. Xu H, Barry DM, Li H, Brunet S, Guo W, Nerbonne JM. 1999. Attenuation of the slow component of delayed rectification, action potential prolongation, and triggered activity in mice expressing a dominant-negative Kv2 α subunit. Circ Res 85:623-633.
116. Xu J, Zhu Y, Heinemann SF. 2006. Identification of sequence motifs that target neuronal nicotinic receptors to dendrites and axons. J Neurosci 26:9780-9793.
117. Yan S, Sanders JM, Xu J, Zhu Y, Contractor A, Swanson GT. 2004. A c-terminal determinant of GLuR6 kainate receptor trafficking. J Neurosci 24:679-691.
118. Yang F, Moss LG, Phillips GN. 1996. The molecular structure of green fluorescent protein. Nat Biotechonol 14:1246-1261.
119. Yu WH, Wolfgang W, Forte M. 1995. Subcellular localization of human voltage-dependent anion channel isoforms. J Biol Chem 270:13998-14006.
120. Yu FH, Westenbroeck RE, Silos-Santiago I, McCormick KA, Lawson D, Ge P, Ferriera H, Lilly J, DiStefano PS, Catterall WA, Scheuer T, Curtis R. 2003. Sodium channel β4, a new disulfide-linked auxilary subunit with similarity to β2. J Neurosci 23:7577-7585.
121. Zerangue N, Schwappach B, Jan YN, Jan LY. 1999. A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane KATP channels. Neuron 22:537-548.
122. Zhang J, Campbell RE, Ting AY, Tsien RY. 2002. Creating new fluorescent probes for cell biology. Nat Rev Mol Cell Biol 3:906-918.
123. Zhang H, Fu Y, Altier C, Platzer J, Surmeier DJ, Bezprozvanny I. 2006. Cav1.2 and Cav1.3 neuronal L-type calcium channels: Differential targeting and sorting to pCREB. Eur J Neurosci 23:2297-2310.
124. Zheng J, Zagotta WN. 2004. Stoichiometry and assembly of olfactory cyclic nucleotide-gated channels. Neuron 42:411-421.
125. +2-binding protein-1 facilitates and forms a postsynaptic complex with Cav1.2 (L type) Ca channels. J Neurosci 24:4698-4708.
126. Zimmer T, Biskup C, Dugarmaa S, Vogel F, Steinbis M, Bohle T, Wu YS, Duamine R, Benndorf K. 2002a. Functional expression of GFP-linked human heart sodium channel (hHI) and subcellular localization of the α subunit on HEK293 cells and dog cardiac myocytes. J Membrane Biol 186:1-12.
127. + channel (hHI) already within the endoplasmic reticulum. J Membrane Biol 186:13-21.