Electron Crystallography and Aquaporins

Methods in Enzymology

Volumn 483, Issue C, 2010, Pages 91-119

  Schenk, Andreas D ^a   Hite, Richard K ^a   Engel, Andreas ^b   Fujiyoshi, Yoshinori ^c   Walz, Thomas ^a,d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c KYOTO UNIVERSITY   (Japan)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN; AQUAPORIN 1; AQUAPORIN 4;

BOOK; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ELECTRON CRYSTALLOGRAPHY; ENZYME ISOLATION; IMAGE ANALYSIS; IMAGE PROCESSING; INFORMATION PROCESSING; INTERMETHOD COMPARISON; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN STRUCTURE; THREE DIMENSIONAL IMAGING; X RAY CRYSTALLOGRAPHY;

EID: 77957234893     PISSN: 00766879     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0076-6879(10)83005-8     Document Type: Chapter

References (122)

1. Agre P., Sasaki S., Chrispeels M.J. Aquaporins: A family of water channel proteins. Am. J. Physiol. 1993, 265:F461.
2. Amos L.A., Henderson R., Unwin P.N. Three-dimensional structure determination by electron microscopy of two-dimensional crystals. Prog. Biophys. Mol. Biol. 1982, 39:183-231.
3. Andrews S., Reichow S.L., Gonen T. Electron crystallography of aquaporins. IUBMB Life 2008, 60:430-436.
4. Bok D., Dockstader J., Horwitz J. Immunocytochemical localization of the lens main intrinsic polypeptide (MIP26) in communicating junctions. J. Cell Biol. 1982, 92:213-220.
5. Booy F.P., Pawley J.B. Cryo-crinkling: What happens to carbon films on copper grids at low temperature. Ultramicroscopy 1993, 48:273-280.
6. Braun T., Philippsen A., Wirtz S., Borgnia M.J., Agre P., Kühlbrandt W., Engel A., Stahlberg H. The 3.7 Å projection map of the glycerol facilitator GlpF: A variant of the aquaporin tetramer. EMBO Rep. 2000, 1:183-189.
7. Calamita G., Bishai W.R., Preston G.M., Guggino W.B., Agre P. Molecular cloning and characterization of AqpZ, a water channel from Escherichia coli. J. Biol. Chem. 1995, 270:29063-29066.
8. Carbrey J.M., Gorelick-Feldman D.A., Kozono D., Praetorius J., Nielsen S., Agre P. Aquaglyceroporin AQP9: Solute permeation and metabolic control of expression in liver. Proc. Natl. Acad. Sci. USA 2003, 100:2945-2950.
9. Casagrande F., Ratera M., Schenk A.D., Chami M., Valencia E., Lopez J.M., Torrents D., Engel A., Palacin M., Fotiadis D. Projection structure of a member of the amino acid/polyamine/organocation transporter superfamily. J. Biol. Chem. 2008, 283:33240-33248.
10. Casagrande F., Harder D., Schenk A., Meury M., Ucurum Z., Engel A., Weitz D., Daniel H., Fotiadis D. Projection structure of DtpD (YbgH), a prokaryotic member of the peptide transporter family. J. Mol. Biol. 2009, 394:708-717.
11. Cheng Y., Walz T. The advent of near-atomic resolution in single-particle electron microscopy. Annu. Rev. Biochem. 2009, 78:723-742.
12. Cheng A., van Hoek A.N., Yeager M., Verkman A.S., Mitra A.K. Three-dimensional organization of a human water channel. Nature 1997, 387:627-630.
13. Crowther R.A., Henderson R., Smith J.M. MRC image processing programs. J. Struct. Biol. 1996, 116:9-16.
14. Daniels M.J., Chrispeels M.J., Yeager M. Projection structure of a plant vacuole membrane aquaporin by electron cryo-crystallography. J. Mol. Biol. 1999, 294:1337-1349.
15. de Groot B.L., Engel A., Grubmüller H. A refined structure of human aquaporin-1. FEBS Lett. 2001, 504:206-211.
16. de Groot B.L., Engel A., Grubmüller H. The structure of the aquaporin-1 water channel: A comparison between cryo-electron microscopy and X-ray crystallography. J. Mol. Biol. 2003, 325:485-493.
17. Deen P.M., Verdijk M.A., Knoers N.V., Wieringa B., Monnens L.A., van Os C.H., van Oost B.A. Requirement of human renal water channel aquaporin-2 for vasopressin-dependent concentration of urine. Science 1994, 264:92-95.
18. Downing K.H. Spot-scan imaging in transmission electron microscopy. Science 1991, 251:53-59.
19. Dunia I., Manenti S., Rousselet A., Benedetti E.L. Electron microscopic observations of reconstituted proteoliposomes with the purified major intrinsic membrane protein of eye lens fibers. J. Cell Biol. 1987, 105:1679-1689.
20. Elkjaer M., Vajda Z., Nejsum L.N., Kwon T., Jensen U.B., Amiry-Moghaddam M., Frøkiaer J., Nielsen S. Immunolocalization of AQP9 in liver, epididymis, testis, spleen, and brain. Biochem. Biophys. Res. Commun. 2000, 276:1118-1128.
21. Engel A., Fujiyoshi Y., Gonen T., Walz T. Junction-forming aquaporins. Curr. Opin. Struct. Biol. 2008, 18:229-235.
22. Fotiadis D., Hasler L., Müller D.J., Stahlberg H., Kistler J., Engel A. Surface tongue-and-groove contours on lens MIP facilitate cell-to-cell adherence. J. Mol. Biol. 2000, 300:779-789.
23. Fraysse L.C., Wells B., McCann M.C., Kjellbom P. Specific plasma membrane aquaporins of the PIP1 subfamily are expressed in sieve elements and guard cells. Biol. Cell 2005, 97:519-534.
24. Fu D., Libson A., Miercke L.J., Weitzman C., Nollert P., Krucinski J., Stroud R.M. Structure of a glycerol-conducting channel and the basis for its selectivity. Science 2000, 290:481-486.
25. Fujiyoshi Y. High resolution cryo-electron microscopy for biological macromolecules. J. Electron Microsc. 1989, 38:97-101.
26. Fujiyoshi Y. The structural study of membrane proteins by electron crystallography. Adv. Biophys. 1998, 35:25-80.
27. Fujiyoshi Y., Unwin N. Electron crystallography of proteins in membranes. Curr. Opin. Struct. Biol. 2008, 18:587-592.
28. Furman C.S., Gorelick-Feldman D.A., Davidson K.G., Yasumura T., Neely J.D., Agre P., Rash J.E. Aquaporin-4 square array assembly: Opposing actions of M1 and M23 isoforms. Proc. Natl. Acad. Sci. USA 2003, 100:13609-13614.
29. Fushimi K., Uchida S., Hara Y., Hirata Y., Marumo F., Sasaki S. Cloning and expression of apical membrane water channel of rat kidney collecting tubule. Nature 1993, 361:549-552.
30. Gipson B., Zeng X., Zhang Z.Y., Stahlberg H. 2dx-User-friendly image processing for 2D crystals. J. Struct. Biol. 2007, 157:64-72.
31. Gipson B., Zeng X., Stahlberg H. 2dx_merge: Data management and merging for 2D crystal images. J. Struct. Biol. 2007, 160:375-384.
32. Glaeser R.M. Specimen flatness of thin crystalline arrays: Influence of the substrate. Ultramicroscopy 1992, 46:33-43.
33. Gomes D., Agasse A., Thiébaud P., Delrot S., Gerós H., Chaumont F. Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochim. Biophys. Acta 2009, 1788:1213-1228.
34. Gonen T., Walz T. The structure of aquaporins. Q. Rev. Biophys. 2006, 39:361-396.
35. Gonen T., Cheng Y., Kistler J., Walz T. Aquaporin-0 membrane junctions form upon proteolytic cleavage. J. Mol. Biol. 2004, 342:1337-1345.
36. Gonen T., Sliz P., Kistler J., Cheng Y., Walz T. Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature 2004, 429:193-197.
37. Gonen T., Cheng Y., Sliz P., Hiroaki Y., Fujiyoshi Y., Harrison S.C., Walz T. Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature 2005, 438:633-638.
38. Gorin M.B., Yancey S.B., Cline J., Revel J.P., Horwitz J. The major intrinsic protein (MIP) of the bovine lens fiber membrane: Characterization and structure based on cDNA cloning. Cell 1984, 39:49-59.
39. Gyobu N., Tani K., Hiroaki Y., Kamegawa A., Mitsuoka K., Fujiyoshi Y. Improved specimen preparation for cryo-electron microscopy using a symmetric carbon sandwich technique. J. Struct. Biol. 2004, 146:325-333.
40. Han B.G., Wolf S.G., Vonck J., Glaeser R.M. Specimen flatness of glucose-embedded biological materials for electron crystallography is affected significantly by the choice of carbon evaporation stock. Ultramicroscopy 1994, 55:1-5.
41. Han B.G., Guliaev A.B., Walian P.J., Jap B.K. Water transport in AQP0 aquaporin: Molecular dynamics studies. J. Mol. Biol. 2006, 360:285-296.
42. Harries W.E., Akhavan D., Miercke L.J., Khademi S., Stroud R.M. The channel architecture of aquaporin 0 at a 2.2-Å resolution. Proc. Natl. Acad. Sci. USA 2004, 101:14045-14050.
43. Hasler L., Walz T., Tittmann P., Gross H., Kistler J., Engel A. Purified lens major intrinsic protein (MIP) forms highly ordered tetragonal two-dimensional arrays by reconstitution. J. Mol. Biol. 1998, 279:855-864.
44. Hasler L., Heymann J.B., Engel A., Kistler J., Walz T. 2D crystallization of membrane proteins: Rationales and examples. J. Struct. Biol. 1998, 121:162-171.
45. Hayward S.B., Glaeser R.M. Radiation damage of purple membrane at low temperature. Ultramicroscopy 1979, 4:201-210.
46. Hayward S.B., Glaeser R.M. High resolution cold stage for the JEOL 100B and 100C electron microscopes. Ultramicroscopy 1980, 5:3-8.
47. Henderson R., Unwin P.N. Three-dimensional model of purple membrane obtained by electron microscopy. Nature 1975, 257:28-32.
48. Henderson R., Baldwin J.M., Ceska T.A., Zemlin F., Beckmann E., Downing K.H. Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J. Mol. Biol. 1990, 213:899-929.
49. Henderson R., Raeburn C., Vigers G. A side-entry cold holder for cryo-electron microscopy. Ultramicroscopy 1991, 35:45-53.
50. Hirai T., Murata K., Mitsuoka K., Kimura Y., Fujiyoshi Y. Trehalose embedding technique for high-resolution electron crystallography: Application to structural study on bacteriorhodopsin. J. Electron Microsc. 1999, 48:653-658.
51. Hirai T., Mitsuoka K., Kidera A., Fujiyoshi Y. Simulation of charge effects on density maps obtained by high-resolution electron crystallography. J. Electron Microsc. 2007, 56:131-140.
52. Hiroaki Y., Tani K., Kamegawa A., Gyobu N., Nishikawa K., Suzuki H., Walz T., Sasaki S., Mitsuoka K., Kimura K., Mizoguchi A., Fujiyoshi Y. Implications of the aquaporin-4 structure on array formation and cell adhesion. J. Mol. Biol. 2006, 355:628-639.
53. Hite R.K., Raunser S., Walz T. Revival of electron crystallography. Curr. Opin. Struct. Biol. 2007, 17:389-395.
54. Hite R.K., Gonen T., Harrison S.C., Walz T. Interactions of lipids with aquaporin-0 and other membrane proteins. Pflugers Arch. 2008, 456:651-661.
55. Hite R.K., Li Z., Walz T. Principles of membrane protein interactions with annular lipids deduced from aquaporin-0 2D crystals. EMBO J. 2010, 29:1652-1658.
56. Hite R.K., Schenk A.D., Li Z., Cheng Y., Walz T. Collecting electron crystallographic data of two-dimensional protein crystals. Methods Enzymol. 2010, 483.
57. Ho J.D., Yeh R., Sandstrom A., Chorny I., Harries W.E., Robbins R.A., Miercke L.J., Stroud R.M. Crystal structure of human aquaporin 4 at 1.8 Å and its mechanism of conductance. Proc. Natl. Acad. Sci. USA 2009, 106:7437-7442.
58. Hub J.S., Grubmüller H., de Groot B.L. Dynamics and energetics of permeation through aquaporins. What do we learn from molecular dynamics simulations?. Handb. Exp. Pharmacol. 2009, 190:57-76.
59. Iacovache I., Biasini M., Kowal J., Kukulski W., Chami M., Van der Goot F.G., Engel A., Rémigy H.W. The 2DX robot: A membrane protein 2D crystallization Swiss army knife. J. Struct. Biol. 2010, 169:370-378.
60. 2 O-channel, AQP-CHIP, in projection at 3.5 Å resolution. J. Mol. Biol. 1995, 251:413-420.
61. Jap B.K., Zulauf M., Scheybani T., Hefti A., Baumeister W., Aebi U., Engel A. 2D crystallization: From art to science. Ultramicroscopy 1992, 46:45-84.
62. Jegerschöld C., Pawelzik S., Purhonen P., Bhakat P., Gheorghe K.R., Gyobu N., Mitsuoka K., Morgenstern R., Jakobsson P.-J., Hebert H. Structural basis for induced formation of the inflammatory mediator prostaglandin E2. Proc. Natl. Acad. Sci. USA 2008, 105:11110-11115.
63. Jensen M.Ø., Dror R.O., Xu H., Borhani D.W., Arkin I.T., Eastwood M.P., Shaw D.E. Dynamic control of slow water transport by aquaporin 0: Implications for hydration and junction stability in the eye lens. Proc. Natl. Acad. Sci. USA 2008, 105:14430-14435.
64. Jiang J., Daniels B.V., Fu D. Crystal structure of AqpZ tetramer reveals two distinct Arg-189 conformations associated with water permeation through the narrowest constriction of the water-conducting channel. J. Biol. Chem. 2006, 281:454-460.
65. Jung J.S., Bhat R.V., Preston G.M., Guggino W.B., Baraban J.M., Agre P. Molecular characterization of an aquaporin cDNA from brain: Candidate osmoreceptor and regulator of water balance. Proc. Natl. Acad. Sci. USA 1994, 91:13052-13056.
66. Khandelia H., Jensen M.Ø., Mouritsen O.G. To gate or not to gate: Using molecular dynamics simulations to morph gated plant aquaporins into constitutively open conformations. J. Phys. Chem. B 2009, 113:5239-5244.
67. Kimura Y., Vassylyev D.G., Miyazawa A., Kidera A., Matsushima M., Mitsuoka K., Murata K., Hirai T., Fujiyoshi Y. Surface of bacteriorhodopsin revealed by high-resolution electron crystallography. Nature 1997, 389:206-211.
68. Kühlbrandt W., Wang D.N., Fujiyoshi Y. Atomic model of plant light-harvesting complex by electron crystallography. Nature 1994, 367:614-621.
69. Kukulski W., Schenk A.D., Johanson U., Braun T., de Groot B.L., Fotiadis D., Kjellbom P., Engel A. The 5 Å structure of heterologously expressed plant aquaporin SoPIP2;1. J. Mol. Biol. 2005, 350:611-616.
70. Landis D.M., Reese T.S. Astrocyte membrane structure: Changes after circulatory arrest. J. Cell Biol. 1981, 88:660-663.
71. Maurel C., Verdoucq L., Luu D.T., Santoni V. Plant aquaporins: Membrane channels with multiple integrated functions. Annu. Rev. Plant Biol. 2008, 59:595-624.
72. Mitra A.K., Yeager M., van Hoek A.N., Wiener M.C., Verkman A.S. Projection structure of the CHIP28 water channel in lipid bilayer membranes at 12-Å resolution. Biochemistry 1994, 33:12735-12740.
73. Mitra A.K., van Hoek A.N., Wiener M.C., Verkman A.S., Yeager M. The CHIP28 water channel visualized in ice by electron crystallography. Nat. Struct. Biol. 1995, 2:726-729.
74. Mitsuoka K., Hirai T., Murata K., Miyazawa A., Kidera A., Kimura Y., Fujiyoshi Y. The structure of bacteriorhodopsin at 3.0 Å resolution based on electron crystallography: Implication of the charge distribution. J. Mol. Biol. 1999, 286:861-882.
75. Mitsuoka K., Murata K., Walz T., Hirai T., Agre P., Heymann J.B., Engel A., Fujiyoshi Y. The structure of aquaporin-1 at 4.5-Å resolution reveals short α-helices in the center of the monomer. J. Struct. Biol. 1999, 128:34-43.
76. Mulders S.M., Preston G.M., Deen P.M., Guggino W.B., van Os C.H., Agre P. Water channel properties of major intrinsic protein of lens. J. Biol. Chem. 1995, 270:9010-9016.
77. 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 2000, 407:599-605.
78. Nedvetsky P.I., Tamma G., Beulshausen S., Valenti G., Rosenthal W., Klussmann E. Regulation of aquaporin-2 trafficking. Handb. Exp. Pharmacol. 2009, 190:133-157.
79. Nielsen S., Nagelhus E.A., Amiry-Moghaddam M., Bourque C., Agre P., Ottersen O.P. Specialized membrane domains for water transport in glial cells: High-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J. Neurosci. 1997, 17:171-180.
80. Nogales E., Wolf S.G., Downing K.H. Structure of the αβ tubulin dimer by electron crystallography. Nature 1998, 391:199-203.
81. Nyblom M., Frick A., Wang Y., Ekvall M., Hallgren K., Hedfalk K., Neutze R., Tajkhorshid E., Törnroth-Horsefield S. Structural and functional analysis of SoPIP2;1 mutants adds insight into plant aquaporin gating. J. Mol. Biol. 2009, 387:653-668.
82. Oshima A., Tani K., Hiroaki Y., Fujiyoshi Y., Sosinsky G.E. Three-dimensional structure of a human connexin26 gap junction channel reveals a plug in the vestibule. Proc. Natl. Acad. Sci. USA 2007, 104:10034-10039.
83. Pao G.M., Wu L.F., Johnson K.D., Höfte H., Chrispeels M.J., Sweet G., Sandal N.N., Saier M.H.J. Evolution of the MIP family of integral membrane transport proteins. Mol. Microbiol. 1991, 5:33-37.
84. Philippsen A., Schenk A.D., Stahlberg H., Engel A. Iplt-Image processing library and toolkit for the electron microscopy community. J. Struct. Biol. 2003, 144:4-12.
85. Philippsen A., Schenk A.D., Signorell G.A., Mariani V., Berneche S., Engel A. Collaborative EM image processing with the IPLT image processing library and toolbox. J. Struct. Biol. 2007, 157:28-37.
86. Preston G.M., Agre P. Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: Member of an ancient channel family. Proc. Natl. Acad. Sci. USA 1991, 88:11110-11114.
87. Preston G.M., Carroll T.P., Guggino W.B., Agre P. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 1992, 256:385-387.
88. Rash J.E., Yasumura T., Hudson C.S., Agre P., Nielsen S. Direct immunogold labeling of aquaporin-4 in square arrays of astrocyte and ependymocyte plasma membranes in rat brain and spinal cord. Proc. Natl. Acad. Sci. USA 1998, 95:11981-11986.
89. Raunser S., Walz T. Electron crystallography as a technique to study the structure of membrane proteins in a lipidic environment. Annu. Rev. Biophys. 2009, 38:89-105.
90. Rémigy H.W., Caujolle-Bert D., Suda K., Schenk A., Chami M., Engel A. Membrane protein reconstitution and crystallization by controlled dilution. FEBS Lett. 2003, 555:160-169.
91. Ren G., Reddy V.S., Cheng A., Melnyk P., Mitra A.K. Visualization of a water-selective pore by electron crystallography in vitreous ice. Proc. Natl. Acad. Sci. USA 2001, 98:1398-1403.
92. Rigaud J.L., Mosser G., Lacapere J.J., Olofsson A., Levy D., Ranck J.L. Bio-Beads: An efficient strategy for two-dimensional crystallization of membrane proteins. J. Struct. Biol. 1997, 118:226-235.
93. Ringler P., Borgnia M.J., Stahlberg H., Maloney P.C., Agre P., Engel A. Structure of the water channel AqpZ from Escherichia coli revealed by electron crystallography. J. Mol. Biol. 1999, 291:1181-1190.
94. Rosenbaum D.M., Rasmussen S.G., Kobilka B.K. The structure and function of G-protein-coupled receptors. Nature 2009, 459:356-363.
95. Sanner M.F., Olson A.J., Spehner J.C. Reduced surface: An efficient way to compute molecular surfaces. Biopolymers 1996, 38:305-320.
96. Savage D.F., Egea P.F., Robles-Colmenares Y., O'Connell J.D.R., Stroud R.M. Architecture and selectivity in aquaporins: 2.5 Å X-ray structure of aquaporin Z. PLoS Biol. 2003, 1:E72.
97. Schenk A.D., Werten P.J., Scheuring S., de Groot B.L., Müller S.A., Stahlberg H., Philippsen A., Engel A. The 4.5 Å structure of human AQP2. J. Mol. Biol. 2005, 350:278-289.
98. Sengupta D., Behera R.N., Smith J.C., Ullmann G.M. The α helix dipole: Screened out?. Structure 2005, 13:849-855.
99. Signorell G.A., Kaufmann T.C., Kukulski W., Engel A., Rémigy H.-W. Controlled 2D crystallization of membrane proteins using methyl-β-cyclodextrin. J. Struct. Biol. 2007, 157:321-328.
100. Silberstein C., Bouley R., Huang Y., Fang P., Pastor-Soler N., Brown D., van Hoek A.N. Membrane organization and function of M1 and M23 isoforms of aquaporin-4 in epithelial cells. Am. J. Physiol. Renal. Physiol. 2004, 287:F501-F511.
101. Stahlberg H., Braun T., de Groot B., Philippsen A., Borgnia M.J., Agre P., Kühlbrandt W., Engel A. The 6.9-Å structure of GlpF: A basis for homology modeling of the glycerol channel from Escherichia coli. J. Struct. Biol. 2000, 132:133-141.
102. Sui H., Han B.G., Lee J.K., Walian P., Jap B.K. Structural basis of water-specific transport through the AQP1 water channel. Nature 2001, 414:872-878.
103. Suzuki H., Nishikawa K., Hiroaki Y., Fujiyoshi Y. Formation of aquaporin-4 arrays is inhibited by palmitoylation of N-terminal cysteine residues. Biochim. Biophys. Acta 2008, 1778:1181-1189.
104. Tani K., Mitsuma T., Hiroaki Y., Kamegawa A., Nishikawa K., Tanimura Y., Fujiyoshi Y. Mechanism of aquaporin-4's fast and highly selective water conduction and proton exclusion. J. Mol. Biol. 2009, 389:694-706.
105. Törnroth-Horsefield S., Wang Y., Hedfalk K., Johanson U., Karlsson M., Tajkhorshid E., Neutze R., Kjellbom P. Structural mechanism of plant aquaporin gating. Nature 2006, 439:688-694.
106. Tsukaguchi H., Shayakul C., Berger U.V., Mackenzie B., Devidas S., Guggino W.B., van Hoek A.N., Hediger M.A. Molecular characterization of a broad selectivity neutral solute channel. J. Biol. Chem. 1998, 273:24737-24743.
107. Unger V.M., Kumar N.M., Gilula N.B., Yeager M. Three-dimensional structure of a recombinant gap junction membrane channel. Science 1999, 283:1176-1180.
108. Unwin P.N., Henderson R. Molecular structure determination by electron microscopy of unstained crystalline specimen. J. Mol. Biol. 1975, 94:425-440.
109. Verbavatz J.M., Ma T., Gobin R., Verkman A.S. Absence of orthogonal arrays in kidney, brain and muscle from transgenic knockout mice lacking water channel aquaporin-4. J. Cell Sci. 1997, 110:2855-2860.
110. Viadiu H., Gonen T., Walz T. Projection map of aquaporin-9 at 7Å resolution. J. Mol. Biol. 2007, 367:80-88.
111. Vonck J. Parameters affecting specimen flatness of two-dimensional crystals for electron crystallography. Ultramicroscopy 2000, 85:123-129.
112. Walz T., Smith B.L., Zeidel M.L., Engel A., Agre P. Biologically active two-dimensional crystals of aquaporin CHIP. J. Biol. Chem. 1994, 269:1583-1586.
113. Walz T., Smith B.L., Agre P., Engel A. The three-dimensional structure of human erythrocyte aquaporin CHIP. EMBO J. 1994, 13:2985-2993.
114. Walz T., Typke D., Smith B.L., Agre P., Engel A. Projection map of aquaporin-1 determined by electron crystallography. Nat. Struct. Biol. 1995, 2:730-732.
115. Walz T., Hirai T., Murata K., Heymann J.B., Mitsuoka K., Fujiyoshi Y., Smith B.L., Agre P., Engel A. The three-dimensional structure of aquaporin-1. Nature 1997, 387:624-627.
116. Walz T., Fujiyoshi Y., Engel A. The AQP structure and functional implications. Handb. Exp. Pharmacol. 2009, 190:31-56.
117. Wang D.N., Kühlbrandt W. High-resolution electron crystallography of light-harvesting chlorophyll a/b-protein complex in three different media. J. Mol. Biol. 1991, 217:691-699.
118. Williams R.C., Glaeser R.M. Ultrathin carbon support films for electron microscopy. Science 1972, 175:1000-1001.
119. Zeidel M.L., Ambudkar S.V., Smith B.L., Agre P. Reconstitution of functional water channels in liposomes containing purified red cell CHIP28 protein. Biochemistry 1992, 31:7436-7440.
120. Zeng X., Stahlberg H., Grigorieff N. A maximum likelihood approach to two-dimensional crystals. J. Struct. Biol. 2007, 160:362-374.
121. Zhao G., Johnson M.C., Schnell J.R., Kanaoka Y., Haase W., Irikura D., Lam B.K., Schmidt-Krey I. Two-dimensional crystallization conditions of human leukotriene C(4) synthase requiring adjustment of a particularly large combination of specific parameters. J. Struct. Biol. 2010, 169:450-454.
122. Zhou Z.H. Towards atomic resolution structural determination by single-particle cryo-electron microscopy. Curr. Opin. Struct. Biol. 2008, 18:218-228.