Determining molecular forces that stabilize human aquaporin-1

Journal of Structural Biology

Volumn 142, Issue 3, 2003, Pages 369-378

  Möller, Clemens ^a   Fotiadis, Dimitrios ^b   Suda, Kitaru ^b   Engel, Andreas ^b   Kessler, Max ^c   Müller, Daniel J ^a,d  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY OF MUNICH   (Germany)

^d DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

Aquaporin; Atomic force microscopy; Force spectroscopy; Membrane protein assembly; Molecular interactions; Secondary structure; Worm like chain model

Indexed keywords

AQUAPORIN 1; MEMBRANE PROTEIN; OLIGOMER;

ARTICLE; ATOMIC FORCE MICROSCOPY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EXTRACTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN STABILITY; PROTEIN STRUCTURE;

EID: 0038779383     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1047-8477(03)00066-2     Document Type: Article

References (46)

1. Binnig G., Quate C.F., Gerber C. Atomic force microscope. Phys. Rev. Lett. 56:1986;930-933.
2. Booth P.J., Templer R.H., Meijberg W., Allen S.J., Curran A.R., Lorch M. In vitro studies of membrane protein folding. Crit. Rev. Biochem. Mol. Biol. 36:2001;501-603.
3. Bustamante C., Marko J.F., Siggia E.D., Smith S. Entropic elasticity of lambda-phage DNA. Science. 265:1994;1599-1600.
4. Butt H.-J., Jaschke M. Calculation of thermal noise in atomic force microscopy. Nanotechnology. 6:1995;1-7.
5. Butt H.-J., Jaschke M., Ducker W. Measuring surface forces in aqueous solution with the atomic force microscope. Bioelectr. Bioenerg. 38:1995;191-201.
6. de Groot B.L., Engel A., Grubmüller H. A refined structure of human aquaporin-1. FEBS Lett. 504:2001;206-211.
7. de Groot B.L., Grubmüller H. Water permeation across biological membranes: mechanism and dynamics of aquaporin-1 and GlpF. Science. 294:2001;2353-2357.
8. Denker B., Smith B., Kuhajda F., Agre P. Identification, purification, and partial characterization of a novel Mr 28,000 integral membrane protein from erythrocytes and renal tubules. J. Biol. Chem. 263:1988;15634-15642.
9. Engel A., Müller D.J. Observing single biomolecules at work with the atomic force microscope. Nat. Struct. Biol. 7:2000;715-718.
10. Evans E. Probing the relation between force-lifetime and chemistry in single molecular bonds. Annu. Rev. Biophys. Biomol. Struct. 30:2001;105-128.
11. Fettiplace R., Haydon D.A. Water permeability of lipid membranes. Physiol. Rev. 60:1980;510-550.
12. 2+ binding domain at the C-terminus of AQP1 J. Mol. Biol. 318:2002;1381-1394.
13. 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. 290:2000;481-486.
14. Grubmüller H., Heymann B., Tavan P. Ligand binding: molecular mechanics calculation of the streptavidin-biotin rupture force. Science. 271:1996;997-999.
15. Heymann J.B., Engel A. Aquaporins: phylogeny, structure, and physiology of water channels. News Physiol. Sci. 14:1999;187-193.
16. Israelachvili J. Intermolecular and Surface Forces. second ed. 1991;Academic Press, London.
17. Jung J.S., Preston G.M., Smith B.L., Guggino W.B., Agre P. Molecular structure of the water channel through aquaporin CHIP. The hourglass model. J. Biol. Chem. 269:1994;14648-14654.
18. Lazaridis T., Karplus M. Effective energy function for proteins in solution. Proteins. 35:1999;133-152.
19. Lu H., Schulten K. Steered molecular dynamics simulations of force-induced protein domain unfolding. Proteins. 35:1999;453-463.
20. Macey R.I., Farmer R.E. Inhibition of water and solute permeability in human red cells. Biochim. Biophys. Acta. 211:1970;104-106.
21. Marko J.F., Siggia E.D. Stretching DNA. Macromolecules. 28:1995;8759-8770.
22. 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. 128:1999;34-43.
23. Müller D.J., Baumeister W., Engel A. Controlled unzipping of a bacterial surface layer with atomic force microscopy. Proc. Natl. Acad. Sci. USA. 96:1999;13170-13174.
24. Müller D.J., Fotiadis D., Scheuring S., Müller S.A., Engel A. Electrostatically balanced subnanometer imaging of biological specimens by atomic force microscopy. Biophys. J. 76:1999;1101-1111.
25. Müller D.J., Janovjak H., Lehto T., Kuerschner L., Anderson K. Observing structure, function and assembly of single proteins by AFM. Prog. Biophys. Mol. Biol. 79:2002;1-43.
26. Müller D.J., Kessler M., Oesterhelt F., Möller C., Pfeiffer M., Oesterhelt D., Gaub H. Assignment of bacteriorhodopsin secondary structure elements by single molecule force spectroscopy. Biophys. J. 82:2002;3578-3588.
27. 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.
28. Oberhauser A.F., Hansma P.K., Carrion-Vazquez M., Fernandez J.M. Stepwise unfolding of titin under force-clamp atomic force microscopy. Proc. Natl. Acad. Sci. USA. 98:2001;468-472.
29. Oesterhelt F., Oesterhelt D., Pfeiffer M., Engel A., Gaub H., Müller D.J. Unfolding pathways of individual bacteriorhodopsins. Science. 288:2000;143-146.
30. Pao G.M., Wu L.F., Johnson K.D., Hofte H., Chrispeels M.J., Sweet G., Sandal N.N., Saier M.H. Jr. Evolution of the MIP family of integral membrane transport proteins. Mol. Microbiol. 5:1991;33-37.
31. Park J.H., Saier M.H. Jr. Phylogenetic characterization of the MIP family of transmembrane channel proteins. J. Membr. Biol. 153:1996;171-180.
32. Popot J.L., Engelman D.M. Membrane protein folding and oligomerization: the two stage model. Biochemistry. 29:1990;4031-4037.
33. Popot J.L., Engelman D.M. Helical membrane protein folding, stability, and evolution. Annu. Rev. Biochem. 69:2000;881-922.
34. 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. 88:1991;11110-11114.
35. Preston G.M., Carroll T.P., Guggino W.B., Agre P. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science. 256:1992;385-387.
36. Radford S.E. Protein folding: progress made and promises ahead. Trends Biochem. Sci. 25:2000;611-618.
37. Rief M., Gautel M., Oesterhelt F., Fernandez J.M., Gaub H.E. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science. 276:1997;1109-1112.
38. Rief M., Oesterhelt F., Heymann B., Gaub H.E. Single molecule force spectroscopy on polysaccharides by atomic force microscopy. Science. 275:1997;1295-1297.
39. Russ W.P., Engelman D.M. The GxxxG motif: a framework for transmembrane helix-helix association. J. Mol. Biol. 296:2000;911-919.
40. Schäffer T.E., Cleveland J.P., Ohnesorge F., Walters D.A., Hansma P.K. Studies of vibrating atomic force microscope cantilevers in liquid. J. Appl. Phys. 80:1996;3622-3627.
41. Sidel V.W., Solomon A.K. Entrance of water into human red blood cells under an osmotic pressure gradient. J. Gen. Physiol. 41:1957;243-257.
42. Smith B.L., Agre P. Erythrocyte Mr 28,000 transmembrane protein exists as a multisubunit oligomer similar to channel proteins. J. Biol. Chem. 266:1991;6407-6415.
43. 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. 414:2001;872-878.
44. Walz T., Smith B.L., Agre P., Engel A. The three-dimensional structure of human erythrocyte aquaporin chip. EMBO J. 13:1994;2985-2993.
45. Walz T., Smith B.L., Zeidel M.L., Engel A., Agre P. Biologically active two-dimensional crystals of aquaporin CHIP. J. Biol. Chem. 269:1994;1583-1586.
46. Zardoya R., Villalba S. A phylogenetic framework for the aquaporin family in eukaryotes. J. Mol. Evol. 52:2001;391-404.