Electrophysiological characterization of membrane transport proteins

Annual Review of Biophysics

Volumn 42, Issue 1, 2013, Pages 95-120

  Grewer, Christof ^a   Gameiro, Armanda ^a   Mager, Thomas ^b   Fendler, Klaus ^b  

^a BINGHAMTON UNIVERSITY   (United States)

^b MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

Author keywords

active transport; caged substrates; charge displacement electrogenic step; conformational transition; rapid kinetics

Indexed keywords

AMINO ACID TRANSPORTER; ANTIPORTER; BICARBONATE CHLORIDE ANTIPORTER; CARRIER PROTEIN; CYTOCHROME C OXIDASE; GLUTAMATE TRANSPORTER; SODIUM PROTON EXCHANGE PROTEIN;

BINDING SITE; BLACK LIPID MEMBRANE; CELL MEMBRANE; CONCENTRATION (PARAMETERS); ELECTRON TRANSPORT; ELECTROPHYSIOLOGY; ESCHERICHIA COLI; LIPID MEMBRANE; MEMBRANE TRANSPORT; MICROELECTRODE; MUTAGENESIS; NONHUMAN; OOCYTE; PATCH CLAMP; POTENTIOMETRY; PRIORITY JOURNAL; PROTON TRANSPORT; REVIEW; SOLID SUPPORTED MEMBRANE; STEADY STATE; STRUCTURE ACTIVITY RELATION; VOLTAGE CLAMP; WHOLE CELL; XENOPUS;

ANIMALS; BACTERIA; BIOLOGICAL TRANSPORT; BIOLOGICAL TRANSPORT, ACTIVE; CELL MEMBRANE; ELECTROPHYSIOLOGICAL PHENOMENA; HUMANS; LIPID BILAYERS; MEMBRANE TRANSPORT PROTEINS; PATCH-CLAMP TECHNIQUES;

EID: 84877789399     PISSN: 1936122X     EISSN: 19361238     Source Type: Book Series    
DOI: 10.1146/annurev-biophys-083012-130312     Document Type: Review

References (106)

1. Adams SR, Tsien RY. 1993. Controlling cell chemistry with caged compounds. Annu. Rev. Physiol. 55:755-844
2. Amara SG. 1992. Neurotransmitter transporters. A tale of two families. Nature 360:420-211
3. Babes A, Fendler K. 2000. Na+ transport, and the E1P-E2P conformational transition of the Na+/K+- ATPase. Biophys. J. 79:2557-711
4. Bastug T, Heinzelmann G, Kuyucak S, Salim M, Vandenberg RJ, Ryan RM. 2012. Position of the third Na+ site in the aspartate transporter GltPh and the human glutamate transporter, EAAT1. PLoS ONE 7:e330588
5. Belevich I, Verkhovsky MI. 2008. Molecular mechanism of proton translocation by cytochrome c oxidase. Antioxid. Redox Signal. 10:1-299
6. Benz R. 2001. Porins - structure and function. In Microbial Transport Systems, ed. G Winkelmann, pp. 227-46. Weinheim, Ger.: Wiley-VCH
7. Bicho A, Grewer C. 2005. Rapid substrate-induced charge movements of the GABA transporter GAT1. Biophys. J. 89:211-311
8. Brandt S, Jentsch TJ. 1995. ClC-6 and ClC-7 are two novel broadly expressed members of the CLC chloride channel family. FEBS Lett. 377:15-200
9. Brett CL, Donowitz M, Rao R. 2005. Evolutionary origins of eukaryotic sodium/proton exchangers. Am. J. Physiol. Cell Physiol. 288:C223-399
10. Bröer S, Schneider H-P, Bröer A, Deitmer JW. 2009. Mutation of asparagine 76 in the center of glutamine transporter SNAT3 modulates substrate-induced conductances and Na+ binding. J. Biol. Chem. 284:25823-311
11. Butt HJ, Fendler K, Der A, Bamberg E. 1989. Temperature jump study of charge translocation during the bacteriorhodopsin photocycle. Biophys. J. 56:851-599
12. Canepari M, Nelson L, Papageorgiou G, Corrie JE, Ogden D. 2001. Photochemical and pharmacological evaluation of 7-nitroindolinyl- and 4-methoxy-7-nitroindolinyl-amino acids as novel, fast caged neurotransmitters. J. Neurosci. Methods 112:29-422
13. Chaudhry FA,ReimerRJ, Krizaj D, Barber D, Storm-Mathisen J, et al. 1999. Molecular analysis of system N suggests novel physiological roles in nitrogen metabolism and synaptic transmission. Cell 99:769-800
14. CleirenE,Benichou O, Van HulE,Gram J,Bollerslev J, et al. 2001. Albers-Schonberg disease (autosomal dominant osteopetrosis, type II) results from mutations in the ClCN7 chloride channel gene. Hum. Mol. Genet. 10:2861-677
15. Collins A, Somlyo AV, Hilgemann DW. 1992. The giant cardiac membrane patch method: Stimulation of outward Na+-Ca2+ exchange current by MgATP. J. Physiol. 454:27-577
16. Counillon L, Pouyssegur J. 2000. The expanding family of eucaryoticNa+/H+ exchangers. J. Biol. Chem. 275:1-44
17. Diamond JS, Jahr CE. 1997. Transporters buffer synaptically released glutamate on a submillisecond time scale. J. Neurosci. 17:4672-877
18. Drachev LA, Jasaitis AA, Kaulen AD, Kondrashin AA, Liberman EA, et al. 1974. Direct measurement of electric current generation by cytochrome oxidase, H+-ATPase and bacteriorhodopsin. Nature 249:321-244
19. Eskandari S, Kreman M, Kavanaugh MP, Wright EM, Zampighi GA. 2000. Pentameric assembly of a neuronal glutamate transporter. Proc. Natl. Acad. Sci. USA 97:8641-466
20. Fang Y, Jayaram H, Shane T, Kolmakova-Partensky L, Wu F, et al. 2009. Structure of a prokaryotic virtual proton pump at 3.2 ̊A resolution. Nature 460:1040-433
21. FendlerK, Jaruschewski S,Hobbs A, AlbersW,Froehlich JP. 1993. Pre-steady-state charge translocation in NaK-ATPase from eel electric organ. J. Gen. Physiol. 102:631-666
22. Ganea C, Fendler K. 2009. Bacterial transporters: Charge translocation and mechanism. Biochim. Biophys. Acta 1787:706-133
23. Gao X, Lu F, Zhou L, Dang S, Sun L, et al. 2009. Structure and mechanism of an amino acid antiporter. Science 324:1565-688
24. Graves AR, Curran PK, Smith CL, Mindell JA. 2008. The Cl/H+ antiporter ClC-7 is the primary chloride permeation pathway in lysosomes. Nature 453:788-922
25. Grewer C, Balani P, Weidenfeller C, Bartusel T, Tao Z, Rauen T. 2005. Individual subunits of the glutamate transporter EAAC1 homotrimer function independently of each other. Biochemistry 44:11913- 233
26. Grewer C, Jager J, Carpenter BK,HessGP. 2000. A new photolabile precursor of glycine with improved properties: A tool for chemical kinetic investigations of the glycine receptor. Biochemistry 39:2063-700
27. Grewer C, Watzke N, Wiessner M, Rauen T. 2000. Glutamate translocation of the neuronal glutamate transporter EAAC1 occurs within milliseconds. Proc. Natl. Acad. Sci. USA 97:9706-111
28. Hamill OP,Marty A, Neher E, Sakmann B, Sigworth FJ. 1981. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 391:85-1000
29. Hatanaka T, Huang W, Wang H, Sugawara M, Prasad PD, et al. 2000. Primary structure, functional characteristics and tissue expression pattern of human ATA2, a subtype of amino acid transport system A. Biochim. Biophys. Acta 1467:1-66
30. HedigerMA, Ikeda T, Coady M, Gundersen CB, Wright EM. 1987. Expression of size-selected mRNA encoding the intestinal Na/glucose cotransporter in Xenopus laevis oocytes. Proc. Natl. Acad. Sci. USA 84:2634-377
31. Henriksen K, Gram J, Neutzsky-Wulff AV, Jensen VK, Dziegiel MH, et al. 2009. Characterization of acid flux in osteoclasts from patients harboring a G215R mutation in ClC-7. Biochem. Biophys. Res. Commun. 378:804-99
32. Hess GP,Grewer C. 1998. Development and application of caged ligands for neurotransmitter receptors in transient kinetic and neuronal circuit mapping studies. Methods Enzymol. 291:443-733
33. Huang Z, Tajkhorshid E. 2010. Identification of the third Na+ site and the sequence of extracellular binding events in the glutamate transporter. Biophys. J. 99:1416-255
34. HunteC, Screpanti M, VenturiM,Rimon A, PadanE,Michel H. 2005. Structure of aNa+/H+ antiporter and insights into mechanism of action and regulation by pH. Nature 534:1197-2022
35. Jack DL, Paulsen IT, Saier MH. 2000. The amino acid/polyamine/ organocation (APC) superfamily of transporters specific for amino acids, polyamines and organocations. Microbiology 146(Pt. 8):1797-8144
36. Kaila VR, VerkhovskyMI, Wikstrom M. 2010. Proton-coupled electron transfer in cytochrome oxidase. Chem. Rev. 110:7062-811
37. Kanai Y, Hediger MA. 1992. Primary structure and functional characterization of a high-affinity glutamate transporter. Nature 360:467-711
38. Kanai Y, Hediger MA. 2004. The glutamate/neutral amino acid transporter family SLC1: Molecular, physiological and pharmacological aspects. Pflugers Arch. 447:469-799
39. Kanner BI, Bendahan A. 1982. Binding order of substrates to the sodium and potassium ion coupled L-glutamic acid transporter from rat brain. Biochemistry 21:6327-300
40. rfsti Kappl M, Hartung K. 1996. Rapid charge translocation by the cardiac Na+-Ca2+ exchanger after a Ca2++
41. concentration jump. Biophys. J. 71:2473-855
42. Kappl M, Nagel G, Hartung K. 2001. Voltage and Ca2+ dependence of pre-steady-state currents of the Na-Ca exchanger generated by Ca2+ concentration jumps. Biophys. J. 81:2628-388
43. Kornak U, Kasper D, Bosl MR, Kaiser E, Schweizer M, et al. 2001. Loss of the ClC-7 chloride channel leads to osteopetrosis in mice and man. Cell 104:205-155
44. Kusano K, Miledi R, Stinnakre J. 1977. Acetylcholine receptors in the oocyte membrane. Nature 270:739-411
45. Laeuger P. 1991. Electrogenic Ion Pumps. Sunderland, MA: Sinauer.
46. Lange PF, Wartosch L, JentschTJ, Fuhrmann JC. 2006. ClC-7 requires Ostm1 as aβ-subunit to support bone resorption and lysosomal function. Nature 440:220-233
47. Leisle L, Ludwig CF, Wagner FA, Jentsch TJ, Stauber T. 2011. ClC-7 is a slowly voltage-gated 2Cl/1H+-exchanger and requires Ostm1 for transport activity. EMBO J. 30:2140-522
48. Levy LM,Warr O, Attwell D. 1998. Stoichiometry of the glial glutamate transporter GLT-1 expressed inducibly in a Chinese hamster ovary cell line selected for low endogenous Na+-dependent glutamate uptake. J. Neurosci. 18:9620-288
49. Lu CC, Hilgemann DW. 1999. GAT1 (GABA:Na+:Cl) cotransport function. Kinetic studies in giant Xenopus oocyte membrane patches. J. Gen. Physiol. 114:445-577
50. Mackenzie B, Erickson JD. 2004. Sodium-coupled neutral amino acid (system N/A) transporters of the SLC38 gene family. Pflugers Arch. 447:784-955
51. rfsti Mager T, Rimon A, Padan E, Fendler K. 2011. Transportmechanism and pHregulation of the Na+/H++ antiporter NhaA from Escherichia coli: An electrophysiological study. J. Biol. Chem. 286:23570-811
52. Marty A, Neher E. 2009. Tight-Seal Whole-Cell Recording. New York: Springer-Verlag
53. Meinild AK, Sitte HH, Gether U. 2004. Zinc potentiates an uncoupled anion conductance associated with the dopamine transporter. J. Biol. Chem. 279:49671-799
54. Mennerick S, ShenW, XuW, Benz A, Tanaka K, et al. 1999. Substrate turnover by transporters curtails synaptic glutamate transients. J. Neurosci. 19:9242-511
55. Meyer-Lipp K, SeryN,Ganea C, Basquin C, Fendler K, LeblancG. 2006. The inner interhelix loop 4-55 of the melibiose permease from Escherichia coli takes part in conformational changes after sugar binding. J. Biol. Chem. 281:25882-922
56. Miller AJ, Zhou JJ. 2000. Xenopus oocytes as an expression system for plant transporters. Biochim. Biophys. Acta 1465:343-588
57. Miller C, Nguitragool W. 2009. A provisional transport mechanism for a chloride channel-type Cl/H+ exchanger. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364:175-800
58. MimC,Tao Z, Grewer C. 2007.Twoconformational changes are associated with glutamate translocation by the glutamate transporter EAAC1. Biochemistry 46:9007-188
59. Neher E, Sakmann B. 1976. Single-channel currents recorded frommembrane of denervated frogmuscle fibres. Nature 260:799-8022
60. Niu L, Vazquez RW, Nagel G, Friedrich T, Bamberg E, et al. 1996. Rapid chemical kinetic techniques for investigations of neurotransmitter receptors expressed in Xenopus oocytes. Proc. Natl. Acad. Sci. USA 93:12964-688
61. Ostermeier C, Harrenga A, Ermler U, Michel H. 1997. Structure at 2.7 ̊A resolution of the Paracoccus denitrificans two-subunit cytochrome c oxidase complexed with an antibody FV fragment. Proc.Natl. Acad. Sci. USA 94:10547-533
62. Otis TS, Jahr CE. 1998. Anion currents and predicted glutamate flux through a neuronal glutamate transporter. J. Neurosci. 18:7099-1100
63. PadanE,Venturi M, Gerchman Y, Dover N. 2001.Na+/H+ antiporters. Biochim. Biophys. Acta 1505:144
64. Pines G, Danbolt NC, Bjoras M, Zhang Y, Bendahan A, et al. 1992. Cloning and expression of a rat brain L-glutamate transporter. Nature 360:464-677
65. Reyes N, Ginter C, Boudker O. 2009. Transport mechanism of a bacterial homologue of glutamate transporters. Nature 462:880-855
66. Rosental N, Gameiro A, Grewer C, Kanner BI. 2011. A conserved aspartate residue located at the extracellular end of the binding pocket controls cation interactions in brain glutamate transporters. J. Biol. Chem. 286:41381-900
67. Ruitenberg M, Kannt A, Bamberg E, Ludwig B, Michel H, Fendler K. 2000. Single-electron reduction of the oxidized state is coupled to proton uptake via the K pathway in Paracoccus denitrificans cytochrome c oxidase. Proc. Natl. Acad. Sci. USA 97:4632-366
68. Sakmann B, Neher E. 2009. Single-Channel Recording. New York: Springer-Verlag.
69. Sauer GA, Nagel G, Koepsell H, Bamberg E, Hartung K. 2000. Voltage and substrate dependence of the inverse transport mode of the rabbit Na+/glucose cotransporter (SGLT1). FEBS Lett. 469:98-1000
70. Schulz P, Garcia-Celma JJ, Fendler K. 2008. SSM-based electrophysiology. Methods 46:97-1033
71. Shaffer PL, Goehring A, Shankaranarayanan A, Gouaux E. 2009. Structure and mechanism of a Na+- independent amino acid transporter. Science 325:1010-144
72. Siletsky S, Kaulen AD, Konstantinov AA. 1999. Resolution of electrogenic steps coupled to conversion of cytochrome c oxidase from the peroxy to the ferryl-oxo state. Biochemistry 38:4853-611
73. Sugawara M, Nakanishi T, Fei YJ, Huang W, Ganapathy ME, et al. 2000. Cloning of an amino acid transporter with functional characteristics and tissue expression pattern identical to that of system A. J. Biol. Chem. 275:16473-777
74. rfsti Taglicht D, Padan E, Schuldiner S. 1991. Overproduction and purification of a functional Na+/H++antiporter coded by nhaA (ant) fromEscherichia coli. J. Biol. Chem. 266:11289-944
75. Taglicht D, Padan E, Schuldiner S. 1993. Proton-sodium stoichiometry of NhaA, an electrogenic antiporter from Escherichia coli. J. Biol. Chem. 268:5382-877
76. Tao Z, Grewer C. 2005. The conserved histidine 295 does not contribute to proton cotransport by the glutamate transporter EAAC1. Biochemistry 44:3466-766
77. Tao Z, Grewer C. 2007. Cooperation of the conserved aspartate 439 and bound amino acid substrate is important for high-affinityNa+ binding to the glutamate transporter EAAC1. J. Gen. Physiol. 129:331-444
78. rfsti Tao Z, Zhang Z, Grewer C. 2006. Neutralization of the aspartic acid residue Asp-367, but not Asp-454, inhibits binding of Na+ to the glutamate-free form and cycling of the glutamate transporter EAAC1.
79. J. Biol. Chem. 281:10263-722
80. Umbach JA, Coady MJ, Wright EM. 1990. Intestinal Na+/glucose cotransporter expressed in Xenopus oocytes is electrogenic. Biophys. J. 57:1217-244
81. Varghese A, Tenbroek EM, Coles J Jr, Sigg DC. 2006. Endogenous channels in HEK cells and potential roles in HCN ionic current measurements. Prog. Biophys. Mol. Biol. 90:26-377
82. Verdon G, Boudker O. 2012. Crystal structure of an asymmetric trimer of a bacterial glutamate transporter homolog. Nat. Struct. Mol. Biol. 19:355-577
83. Verkhovsky MI, Tuukkanen A, Backgren C, Puustinen A, Wikstrom M. 2001. Charge translocation coupled to electron injection into oxidized cytochrome c oxidase from Paracoccus denitrificans. Biochemistry 40:7077-833
84. Wadiche JI, Amara SG, Kavanaugh MP. 1995. Ion fluxes associated with excitatory amino acid transport. Neuron 15:721-288
85. Wadiche JI, Arriza JL, Amara SG, Kavanaugh MP. 1995. Kinetics of a human glutamate transporter. Neuron 14:1019-277
86. Wadiche JI, Kavanaugh MP. 1998. Macroscopic and microscopic properties of a cloned glutamate transporter/chloride channel. J. Neurosci. 18:7650-611
87. Wagner CA, Friedrich B, Setiawan I, Lang F, Broer S. 2000. The use of Xenopus laevis oocytes for the functional characterization of heterologously expressed membrane proteins. Cell Physiol. Biochem. 10:1-122
88. Wartosch L, Fuhrmann JC, Schweizer M, Stauber T, Jentsch TJ. 2009. Lysosomal degradation of endocytosed proteins depends on the chloride transport protein ClC-7. FASEB J. 23:4056-688
89. Watzke N, Bamberg E, Grewer C. 2001. Early intermediates in the transport cycle of the neuronal excitatory amino acid carrier EAAC1. J. Gen. Physiol. 117:547-622
90. Watzke N, Grewer C. 2001. The anion conductance of the glutamate transporter EAAC1 depends on the direction of glutamate transport. FEBS Lett. 503:121-255
91. Watzke N, Rauen T, Bamberg E, Grewer C. 2000. On the mechanism of proton transport by the neuronal excitatory amino acid carrier 1. J. Gen. Physiol. 116:609-222
92. Weinert S, Jabs S, Supanchart C, Schweizer M, Gimber N, et al. 2010. Lysosomal pathology and osteopetrosis upon loss of H+-driven lysosomal Cl accumulation. Science 328:1401-33
93. Wieboldt R, Gee KR, Niu L, Ramesh D, Carpenter BK, Hess GP. 1994. Photolabile precursors of glutamate: Synthesis, photochemical properties, and activation of glutamate receptors on a microsecond time scale. Proc. Natl. Acad. Sci. USA 91:8752-566
94. Wright EM, Loo DD, Panayotova-HeiermannM, LostaoMP, Hirayama BH, et al. 1994. 'Active' sugar transport in eukaryotes. J. Exp. Biol. 196:197-2122
95. Wuddel I, Apell HJ. 1995. Electrogenicity of the sodium transport pathway in theNa,K-ATPase probed by charge-pulse experiments. Biophys. J. 69:909-211
96. Yao D, Mackenzie B, Ming H, Varoqui H, Zhu H, et al. 2000. A novel system A isoform mediating Na+/neutral amino acid cotransport. J. Biol. Chem. 275:22790-977
97. Yernool D, Boudker O, Jin Y, Gouaux E. 2004. Structure of a glutamate transporter homologue from Pyrococcus horikoshii. Nature 431:811-188
98. Yerushalmi H, Schuldiner S. 2000. A model for coupling of H+ and substrate fluxes based on "timesharing"; of a common binding site. Biochemistry 39:14711-199
99. Zerangue N, Kavanaugh MP. 1996. Flux coupling in a neuronal glutamate transporter. Nature 383:634-377
100. Zhang Z, Albers T, Fiumera HL, Gameiro A, Grewer C. 2009. A conserved Na+ binding site of the sodium-coupled neutral amino acid transporter 2 (SNAT2). J. Biol. Chem. 284:25314-233
101. rfsti Zhang Z, Gameiro A, Grewer C. 2008. Highly conserved asparagine 82 controls the interaction of Na++ with the sodium-coupled neutral amino acid transporter SNAT2. J. Biol. Chem. 283:12284-922
102. Zhang Z, Grewer C. 2007. The sodium-coupled neutral amino acid transporter SNAT2 mediates an anion leak conductance that is differentially inhibited by transported substrates. Biophys. J. 92:2621-322
103. Zhang Z, Papageorgiou G, Corrie JE, Grewer C. 2007. Pre-steady-state currents in neutral amino acid transporters induced by photolysis of a new caged alanine derivative. Biochemistry 46:3872-800
104. Zhang Z, Tao Z, Gameiro A, Barcelona S, Braams S, et al. 2007. Transport direction determines the kinetics of substrate transport by the glutamate transporterEAAC1. Proc.Natl. Acad. Sci. USA104:18025- 300
105. Zuber D, Krause R, Venturi M, Padan E, Bamberg E, Fendler K. 2005. Kinetics of charge translocation in the passive downhill uptake mode of the Na+/H+ antiporter NhaA of Escherichia coli. Biochim. Biophys. Acta 1709:240-500
106. Mwaura J, Tao Z, James H, Albers T, Schwartz A, Grewer C. 2012. Protonation state of a conserved acidic amino acid involved in Na+ binding to the glutamate transporter EAAC1. ACS Chem. Neurosci. 3(12):1073-83vv