Forging the link between structure and function of electrogenic cotransporters: The renal type IIa Na+/Pi cotransporter as a case study

Progress in Biophysics and Molecular Biology

Volumn 80, Issue 3, 2002, Pages 69-108

  Forster, Ian C ^a   Köhler, Katja ^a   Biber, Jürg ^a   Murer, Heini ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Cotransporters; Electrophysiology; Structure function; Transport kinetics

Indexed keywords

CARRIER PROTEIN; PHOSPHATE; PHOSPHORUS; SODIUM; SODIUM ION;

AMINO ACID SEQUENCE; ANIMAL; ASSAY; BIOCHEMISTRY; BIOLOGICAL MODEL; CELL MEMBRANE TRANSPORT; CHEMICAL MODEL; CHIMERA; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; HUMAN; ION TRANSPORT; KIDNEY; KINETICS; METABOLISM; MODEL; MOLECULAR BIOLOGY; MOLECULAR GENETICS; NONHUMAN; PH; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; REVIEW; SEQUENCE HOMOLOGY; SODIUM TRANSPORT; STEADY STATE; STOICHIOMETRY; STRUCTURE ACTIVITY RELATION; TRANSPORT AT THE CELLULAR LEVEL; VALIDATION PROCESS;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; HYDROGEN-ION CONCENTRATION; ION TRANSPORT; KIDNEY; KINETICS; MODELS, BIOLOGICAL; MODELS, CHEMICAL; MOLECULAR SEQUENCE DATA; PHOSPHATES; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; SEQUENCE HOMOLOGY, AMINO ACID; SODIUM; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 0036837356     PISSN: 00796107     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0079-6107(02)00015-9     Document Type: Review

References (147)

1. Adrian R.H. Charge movement in the membrane of striated muscle. Ann. Rev. Biophys. Bioeng. 7:1978;85-112.
2. Bezanilla F. The voltage sensor in voltage-dependent ion channels. Physiol. Rev. 80:2000;555-592.
3. Biber J. Emerging roles of transporter-PDZ complexes in renal proximal tubular reabsorption. Pflüegers Arch. 443:2002;3-5.
4. Bibi E., Kaback H.R. In vivo expression of the lacY gene in two segments leads to functional lac permease. Proc. Natl. Acad. Sci. USA. 87:1990;4325-4329.
5. +/glucose cotransporter cloned from rabbit small intestine. Pflüegers Arch. 418:1991;70-85.
6. Bossi E., Centinaio E., Castagna M., Giovannardi S., Vincenti S., Sachhi V.F., Peres A. Ion binding and permeation through the lepidoteran amino acid transporter KAAT1 expressed in Xenopus oocytes. J. Physiol. 515:1999;729-742.
7. Brocke L., Bendahan A., Grunewald M., Kanner B.I. Proximity of two oppositely oriented reentrant loops in the glutamate transporter GLT-1 identified by paired cysteine mutagenesis. J. Biol. Chem. 277:2002;3985-3992.
8. i-cotransport mediated by a transporter cloned from rat kidney and expressed in Xenopus oocytes. Proc. Natl. Acad. Sci. USA. 91:1994;8205-8208.
9. i transporter. J. Am. Soc. Nephrol. 6:1995;1547-1551.
10. +:glucose coupling ratio for the human SGLT1 cotransporter. Biophys. J. 69:1995;2405-2414.
11. +-glucose cotransporter. Biophys. J. 71:1996;2544-2552.
12. +-glucose cotransporter. Biophys. J. 73:1997;2503-2510.
13. +/glucose and Na+/myo-inositol cotransporters. Biochem. Biophys. Acta, 1466:2000;139-150.
14. i cotransport in rat kidney. localization by RT-PCR and immunohistochemistry Am. J. Physiol. 266:1994;F767-F774.
15. +/glutamate symport carrier gene of Escherichia coli B. J. Biol. Chem. 265:1990;21704-21708.
16. i cotransporter. J. Biol. Chem. 275:2000;6284-6287.
17. i cotransporters expressed in Xenopus oocytes. J. Physiol. 531:2001;383-391.
18. Délisle M.-C., Vachon V., Giroux S., Potier M., Boyer C., Laprade R., Béliveau R. Molecular size of the renal sodium/phosphate symporter in native and reconstituted systems. Biochim. Biophys. Acta. 1104:1992;132-136.
19. Délisle M.-C., Giroux S., Vachon V., Boyer C., Potier M., Béliveau R. Molecular size of the functional complex and protein subunits of the renal phosphate symporter. Biochemistry. 33:1994;9105-9109.
20. + conduction and selectivity Science. 280:1998;69-77.
21. Dutzler R., Campbell E.B., Cadene M., Chait B.T., MacKinnon R. X-ray structure of a ClC chloride channel at 3.0 A reveals the molecular basis of anion selectivity. Nature. 415:2002;287-294.
22. i-cotransporter. J. Membr. Biol., in press.
23. Erlinder F., Männikkö R., Larsson H.P. S4 charges move close to residues in the pore domain during activation in a K channel. J. Gen. Physiol. 118:2001;1-10.
24. - symporter. Mechanisms, stoichiometry and specificity J. Biol. Chem. 272:1997;27230-27238.
25. Eskandari S., Wright E.M., Kreman M., Starace D.M., Zampighi G. Structural analysis of cloned plasma membrane proteins by freeze-fracture electron microscopy. Proc. Natl. Acad. Sci. USA. 95:1998;11235-11240.
26. Eskandari, S., Loo, D.D.F., Wright, E.M., 1999. Functional asymmetry of the sodium/glucose cotransporter. Experimental Biology 99, Washington, DC; FASEB J. 13, A399.
27. Eskandari S., Kreman M., Kavanaugh M.P., Wright E.M., Zampighi G.A. The pentameric assembly of a neuronal glutamate transporter. Proc. Natl. Acad. Sci. USA. 97:2000;8641-8646.
28. Falk S., Guay A., Chenu C., Patil S.D., Berteloot A. Reduction of an eight-state mechanism of cotransport to a six-state model using a new computer program. Biophys. J. 74:1998;816-830.
29. Fedida D., Hesketh J.C. Gating of voltage-dependent potassium channels. Prog. Biophys. Mol. Biol. 75:2001;165-199.
30. Feild J.A., Zhang L., Brun K.A., Broooks D.P., Edwards R.M. Cloning and functional characterization of a sodium-dependent phosphate transporter expressed in human lung and small intestine. Biochem. Biophys. Res. Comm. 258:1999;578-582.
31. Firsov D., Gautschi I., Merillat A.M., Rossier B.C., Schild L. The heterotetrameic architecture of the epithelial sodium channel (EnaC). EMBO J. 17:1998;344-352.
32. i cotransporter (NaPi-5) expressed in Xenopus laevis oocytes. J. Membr. Biol. 160:1997;9-25.
33. i cotransporter (NaPi-2). J. Gen. Physiol. 112:1998;1-18.
34. i cotransporters. Am. J. Physiol. 276:1999;F644-F649.
35. i cotransporter. Biophys. J. 79:2000;215-230.
36. i contraporter kinetics by the arginine modifier phenylglyoxal. J. Membr. Biol. 187:2002;85-96.
37. i cotransporter reveal a unique kinetic behavior. Pflüegers Arch. 443 (Suppl.) (abstract P23-4), 284.
38. Frillingos S., Sahin-Toth M., Wu J., Kaback H.R. Cys-scanning mutagenesis. A novel approach to structure-function relationships in polytopic membrane proteins FASEB J. 12:1998;1281-1299.
39. Fu D., Libson A., Miercke L.J., Weitzmann C., Nollert P., Krucinski J., Stroud R.M. Structure of a glycerol conducting channel and the basis for its selectivity. Science. 290:2000;481-486.
40. Gottschalk C.W., Lassiter W.E., Mylle M. Localization of urine acidification in the mammalian kidney. Am. J. Physiol. 198:1960;581-585.
41. Graham, C., Nalbant, P., Schölermann, B., Hentschel, H., Kinne, R.H.K., Werner, A., 2002. Molecular cloning of a novel Na/Pi cotransporter from zebrafish kidney. Pflüegers Arch. 443 (Suppl.) (abstract P23-5), 284.
42. Grunewald M., Kanner B.I. The accessibility of a novel reentrant loop of the glutamate transporter GLT-1 is restricted by its substrate. J. Biol. Chem. 275:2000;9684-9689.
43. +/myo-inositol cotransporter expressed in Xenopus oocytes. J. Membr. Biol. 143:1995;103-113.
44. i-cotransporter. Pflüegers Arch. 430:1995;830-836.
45. i cotransport. J. Biol. Chem. 39:1994;24143-24149.
46. +/glucose cotransporter (SGLT1). J. Membr. Biol. 155:1998;175-186.
47. +/glucose cotransporter. Nature. 330:1987;379-381.
48. Heymann J.A.W., Sarker R., Hirai T., Shi D., Milne J.L.S., Maloney P.C., Subramanian S. Projection structure and molecular architecture of Ox1T, a bacterial membrane transporter. EMBO J. 20:2001;4408-4413.
49. -) cotransport function. database reconstruction with an alternating access model J. Gen. Physiol. 114:1999;459-475.
50. Hilfiker H., Hattenhauer O., Traebert M., Forster I., Murer H., Biber J. Characterization of a new murine type II sodium-phosphate cotransporter expressed in mammalian small intestine. Proc. Natl. Acad. Sci. USA. 95:1998;14564-14569.
51. +/glucose cotransporter (SGLT1). J. Biol. Chem. 269:1994;21407-21410.
52. Holmgren M., Liu Y., Xu Y., Yellen G. On the use of thiol-modifying agents to determine channel topology. Neuropharmacology. 35:1996;97-804.
53. + channel. J. Gen. Physiol. 115:2000;51-58.
54. Javitch J.A. Probing structure of neurotransmitter transporters by substituted-cysteine accessibility method. Methods Enzymol. 286:1998;332-346.
55. Kaback R.H., Sahin-Toth M., Weinglass A.B. The kamikaze approach to membrane transport. Nat. Rev. Mol. Cell Biol. 2:2001;610-620.
56. Kamdar G., Penado K.M.Y., Rudnick G., Stephan M.M. Functional role of critical stripe residues in transmembrane span 7 of the serotonin transporter. J. Biol. Chem. 276:2001;4038-4045.
57. Kaplan R.S. Structure and function of mitochondrial anion transport proteins. J. Membr. Biol. 179:2001;165-183.
58. Karlin A., Akabas M.H. Substituted-cysteine accessibility method. Methods Enzymol. 293:1998;123-145.
59. Kavanaugh M.P., Miller D.G., Zhang W., Law W., Kozak S.L., Kabat D., Miller A.D. Cell-surface receptors for gibbon ape leukemia virus an amphotropic murine retrovirus are inducible sodium-dependent phosphate symporters. Proc. Natl. Acad. Sci. USA. 91:1994;7071-7075.
60. +, D-glucose cotransporter. an asymmetric gated channel (or pore) responsive to ΔΨ. J. Membr. Biol. 76:1983;27-56.
61. Kohl B., Huelsweh B., Elger M., Hentschel H., Kinne R.K.H. Na-Pi cotransport in flounder. Same system in kidney and intestine Am. J. Physiol. Renal Electrolyte Physiol. 270:1996;F937-F944.
62. i-II) with a cleaved protein backbone. implications on function and membrane insertion J. Physiol. 508:1998;341-350.
63. i cotransporter is a monomer. J. Biol. Chem. 275:2000;26113-26120.
64. Kohler K., Forster I.C., Stange G., Biber J., Murer H. Identification of functionally important sites in the first intracellular loop of the NaPi-IIa cotransporter. Am. J. Physiol. Renal Physiol. 282:2002;F687-F696.
65. i cotransporter codetermine a putative transport pathway. Pflüegers Arch. 443 (Suppl.) (abstract P23-7), 285.
66. i cotransporter protein. J. Gen. Physiol. 114:1999;637-651.
67. Lambert G., Traebert M., Hernando N., Biber J., Murer M. Studies on the topology of the renal type II NaPi-cotransporter. Pflüegers Arch. 437:1999;972-978.
68. Lambert G., Forster I.C., Biber J., Murer H. Cysteine residues and the structure of the rat renal proximal tubular type II sodium phosphate cotransporter (rat NaPi-IIa). J. Membr. Biol. 176:2000;133-141.
69. I cotransporter. J. Gen. Physiol. 117:2001;533-546.
70. Läuger P., Jauch P. Ion-driven transport systems. J. Membr. Biol. 91:1986;275-284.
71. Li M., Farley R.A., Lester H.A. An intermediate state of the γ-aminobutyric acid transporter GAT1 revealed by simultaneous voltage clamp and fluorescence. J. Gen. Physiol. 115:2000;491-508.
72. +/glucose contransporter SGLT1. J. Biol. Chem. 273:1998;29341-29351.
73. +/glucose cotransporter. Proc. Natl. Acad. Sci. USA. 90:1993;5767-5771.
74. +/glucose cotransporter. FASEB J. 8:1994;A344.
75. + and glucose transport. Proc. Natl. Acad. Sci. USA. 95:1998;7789-7794.
76. Loo, D.D.F., Eskandari, S., Hirayama, B.A., Wright, E.M., 2002. A kinetic model for secondary active transport. In: Layton, H. E., Weinstein, A. M. (Eds.), IMA Volumes in Mathematics and its Applications, Vol. 129: Membrane Transport and Renal Physiology. Springer, New York, in press.
77. -) cotransport function. steady state studies in giant Xenopus oocyte membrane patches J. Gen. Physiol. 114:1999;429-444.
78. -) cotransport function. Kinetic studies in giant Xenopus oocyte membrane patches J. Gen. Physiol. 114:1999;445-457.
79. Lu C.-C., Kabakov A., Markin V.S., Mager S., Frazier G.A., Hilgemann D.W. Membrane transport mechanisms probed by capacitance measurements with megahertz voltage clamp. Proc. Natl. Acad. Sci. USA. 92:1995;11220-11224.
80. +-coupled oligopeptide transporter hPEPT1. J. Biol. Chem. 271:1996;5430-5437.
81. +/glucose cotransporter (SGLT1) currents and fluxes. J. Membr. Biol. 162:1998;101-106.
82. MacKinnon R. Determination of the subunit stoichiometry of a voltage-activated potassium channel. Nature. 350:1991;232-235.
83. MacKinnon R. Pore loops. an emerging theme in ion channel structure Neurone. 4:1995;889-892.
84. Magagnin S., Werner A., Markovich D., Sorribas V., Stange G., Biber J., Murer H. Expression cloning of human and rat renal cortex Na/Pi cotransport. Proc. Natl. Acad. Sci. USA. 90:1993;5979-5983.
85. Mager S., Naeve J., Quick M., Labarca C., Davidson N. , Lester H.A. Steady states, charge movements, and rates for a cloned GABA transporter expressed in Xenopus oocytes. Neurone. 10:1993;177-188.
86. +/glucose cotransporter. Biochemistry. 40:2001;11897-11904.
87. +/glucose cotransporter. Biochemistry. 41:2002;1250-1258.
88. Mitrovic A.D., Amara S.G., Johnston G.A.R., Vandenberg R.J. Identification of functional domains of the human glutamate transporters EAAT1 and EAAT2. J. Biol. Chem. 273:1998;14698-14706.
89. Murata K., Mitsuoka K., Hirai T., Walz T., Agre P., Heymann J.B., Engel A., Fujiyoshi Y. Structural determinants of water permeation through aquaporin-1. Nature. 407:2000;599-605.
90. Murer H., Biber J. Molecular mechanisms of renal apical Na/phosphate cotransport. Annu. Rev. Physiol. 58:1996;607-618.
91. Murer H., Hernando N., Forster I., Biber J. Proximal tubular phosphate reabsorption. molecular mechanisms Physiol. Rev. 80:2000;1373-1409.
92. +-phosphate cotransporter (NaPi-II) from zebra fish and indentification of related transcripts. J. Physiol. 520:1999;79-89.
93. 2+ exchanger. J. Biol. Chem. 274:1999;910-917.
94. Olah Z., Lehel C., Anderson W.B., Eiden M.V., Wilson C.A. The cellular receptor for gibbon ape leukemia virus is a novel high affinity sodium-dependent phosphate transporter. J. Biol. Chem. 41:1994;25426-25431.
95. 2+ exchangers. J. Biol. Chem. 276:2001;19603-19609.
96. +/sulfate cotransporters is located in the carboxy-terminal portion of the protein. Biochim. Biophys. Acta. 1370:1998;98-106.
97. +/dicarboxylate cotransporter. J. Biol. Chem. 273:1998;18923-18929.
98. +/glucose cotransporters is determined by the carboxy-terminal half of the protein. J. Biol. Chem. 271:1996;10029-10034.
99. +/glucose cotransporter. J. Biol. Chem. 272:1997;20324-20327.
100. +/glucose cotransporter (SGLT1) expressed in E. coli. FEBS Lett. 459:1999;386-390.
101. +/glucose contransporter. I voltage clamp studies J. Membr. Biol. 125:1992;49-62.
102. +/glucose contransporter. II a transport model under nonrapid equilibrium conditions J. Membr. Biol. 125:1992;63-69.
103. Philipson K.D., Nicoll D.A. Sodium-calcium exchange. a molecular perspective Annu. Rev. Physiol. 62:2000;111-133.
104. Press, W.H., Flannery, B.P., Teukolsky, S.A., Vetterling, W.T., 1992. Numerical Recipes in C. Cambridge University Press, Cambridge, UK, pp. 382-397.
105. 2+ exchanger. J. Biol. Chem. 276:2001;194-199.
106. Qui Z., Chen J., Nicoll D.A., Philipson K.D. A disulfide bond is required for functional assembly of NCX1 from complementary fragments. Biochem. Biophys. Res. Comm. 287:2001;825-828.
107. Rosenberg M.F., Mao Q., Holzenburg A., Ford R.C., Deeley R.G., Cole S.P.C. The structure of the multidrug resistance protein 1 (MRP1/ABCC1). J. Biol. Chem. 276:2001;16076-16082.
108. Sahin-Toth M., Lawrence M.C., Kaback H.R. Properties of permease dimer, a fusion protein containing two lactose permease molecules from E. coli. Proc. Natl. Acad. Sci. USA. 91:1994;5421-5425.
109. Sato S., Ueno Y., Asai K., Takahashi K., Sato M., Engel A., Fujiyoshi Y. The voltage-sensitive sodium channel is a bell-shaped molecule with several cavities. Nature. 409:2001;1047-1051.
110. +/glucose cotransporter (SGLT1). FEBS Lett., 469:2000;98-100.
111. Schmidt-Rose T., Jentsch T.J. Reconstitution of functional voltage-gated chloride channels from complementary fragments of CLC-1. J. Biol. Chem. 272:1997;20515-20521.
112. Schwarz E.M., Benzer S. Calx, a Na-Ca exchanger gene of drosophila melanogaster. Proc. Natl. Acad. Sci. USA. 94:1997;10249-10254.
113. Seal R.P., Leighton B.H., Amara S.G. A model for the topology of excitatory amino acid transporters determined by the extracellular accessibility of substituted cysteines. Neurone. 25:2000;695-706.
114. Segawa H., Kaneko I., Takahashi A., Kuwahata M., Ito M., Ohkido I., Tatsumi S., Miyamoto K. Growth-related renal type II Na/Pi cotransporter. J. Biol. Chem. 277:2002;19665-19672.
115. Segel I.H. Enzyme Kinetics. 1975;Wiley, New York.
116. +/glucose cotransporter Seldin D. W., Giebisch G. The Kidney, Physiology and Pathophysiology. 2000;2167-2177 Raven, New York.
117. Slotboom D.J., Konings W.N., Lolkema J.S. The structure of glutamate transporters shows channel-like features. FEBS Lett. 492:2001;183-186.
118. Sonders M.S., Amara S.G. Channels in transporters. Curr. Opinion Neurobiol. 6:1996;294-302.
119. Sorribas V., Markovich D., Hayes G., Stange G., Forgo J., Biber J., Murer H. Cloning of Na/Pi cotransporter from opossum kidney cells. J. Biol. Chem. 269:1994;6615-6621.
120. + channel. J. Gen. Physiol. 117:2001;469-490.
121. Stevens B.R., Fernandez A., Hirayama B., Wright E.M., Kempner E.S. Intestinal brush border membrane Na+/glucose cotransporter functions in situ as a homotetramer. Proc. Natl. Acad. Sci. USA. 87:1990;1456-1460.
122. Su A., Mager S., Mayo S.L., Lester H.A. A multi-substrate single-file model for ion-coupled transporters. Biophys. J. 70:1996;762-777.
123. Taglialatela M., Toro L., Stefani E. Novel voltage clamp to record small, fast currents from ion channels expressed in Xenopus oocytes. Biophys. J. 61:1992;78-82.
124. +-dependent phosphate cotransporter (NaPi-2) in rat kidney. J. Biol. Chem. 273:1998;28568-28575.
125. +-dependent L-ascorbic acid transporters. Nature. 399:1999;70-75.
126. +/glucose cotransporter expressed in Xenopus oocytes is electrogenic. Biophys. J. 57:1990;1217-1224.
127. Unwin N. The Croonian lecture 2000. Nicotinic acetylcholine receptor and the structural basis of fast synaptic transmission. Philos. Trans. R. Soc. London B. 355:2000;1813-1829.
128. Wadiche J.I., Arriza J.L., Amara S.G., Kavanaugh M.P. Kinetics of a human glutamate transporter. Neurone. 14:1995;1019-1027.
129. Wadiche J.I., Amara S.G., Kavanaugh M.P. Ion fluxes associated with excitatory amino acid transport. Neurone. 15:1995;721-728.
130. Wang L., Groves J.D., Mawby W.J., Tanner M.J.A. Complementation studies with co-expressed fragments of the human red cell anion transporter (Band 3; AE1). J. Biol. Chem. 272:1997;10631-10638.
131. Watzke N., Bamberg E., Grewer C. Early intermediates in the transport cycle of the neuronal excitatory amino acid carrier EAAC1. J. Gen. Physiol. 117:2001;547-562.
132. Weiss J.N. The Hill equation revisited. uses and misuses FASEB J. 11:1997;835-841.
133. i cotransport systems. Am. J. Physiol. Regulatory Integrative Comp. Physiol. 280:2001;R301-R312.
134. Werner A., Moore M.L., Mantei N., Biber J., Semenza G., Murer H. Cloning and expression of cDNA for a Na/Pi cotransport system of kidney cortex. Proc. Natl. Acad. Sci. USA. 88:1991;9608-9612.
135. Werner A., Murer H., Kinne R.K.H. Cloning and functional expression of a renal Na-Pi cotransport system from flounder. Am. J. Physiol. 267:1994;F311-F317.
136. Williams K. Three-dimensional structure of the ion-coupled transport protein NhaA. Nature. 403:2000;112-115.
137. Williams K.A., Geldmacher-Kaufer U., Padan E., Shuldiner S., Kühlbrandt W. Projection structure of NhaA, a secondary transporter from E. coli at 4. Å resolution EMBO J. 18:1999;3558-3563.
138. Wolfram S. Mathematica. A System for doing Mathematics by Computer:1993;Addison-Wesley, New York.
139. Wu J., Kaback H.R. Helix proximity and ligand-induced conformational changes in the lactose permease of E. coli determined by site-directed chemical crosslinking. J. Mol. Biol. 270:1997;285-293.
140. Xiao Y., Boyer C.J.-C., Vincent E., Dugre A., Vachon V., Potier M., Béiveau R. Involvement of disulphide bonds in the renal sodium/phosphate co-transporter NaPi-2. Biochem. J. 323:1997;401-408.
141. +/glucose cotransporter. J. Biol. Chem. 275:2000;25959-25964.
142. Yao X., Pajor A.M. The transport properties of the human renal Na+-dicarboxylate cotransporter under voltage clamp conditions. Am. J. Physiol. Renal Physiol. 279:2000;F54-F64.
143. Yin C.C., Aldema-amos M.L., Borges-Walmsey M.I., Taylor R.W., Walmsey A.R., Levy S.B., Bullough P.A. The quaternary molecular structure of TetA, a secondary tetracycline transporter from E. coli. Mol. Microbiol. 38:2000;482-492.
144. Zampighi G.A., Kreman M., Boorer K.J., Loo D.D.F., Bezanilla F., Chandy G., Hall J.E., Wright E.M. A method for determining the unitary functional capacity of cloned channels and transporters expressed in Xenopus laevis oocytes. J. Membr. Biol. 148:1995;65-78.
145. Zen K.H., McKenna E., Bibi E., Hardy D., Kaback H.R. Expression of lactose permease in contiguous fragments as a probe for membrane-spanning domains. Biochemistry. 33:1994;8198-8206.
146. Zhang H., Karlin A. Identification of acetylcholine receptor channel-lining residues in the M1 segment of the β-subunit. Biochemistry. 36:1997;15856-15864.
147. Zhuang J., Prive G.P., Werner G.E., Ringler P., Kaback H.R., Engel A. Two-dimensional crystallization of E. coli lactose permease. J. Struct. Biol. 125:1998;63-75.