Abstract
Water channels are the subject of much current attention, as they may be central for cell functions in a host of tissues. We have analyzed the possible fold of facilitators and water channels of the MIP family based on structural predictions, on findings about the topology of CHIP28, and on the biophysical characteristics of water channels. We developed predictions for the following proteins: MIP26, NOD26, GLP, BIB, γ-TIP, FA-CHIP, CHIP28k, WCH-CD1, and CHIP28. We utilized Kyte Doolittle hydrophobicity, Eisenberg's amphiphilicity, Chou-Fasman-Prevelige propensities, and our own Union algorithm. We found that hydrophobic amphiphilic segments likely to be transmembrane were consistently shorter than required for α-helical segments, but of the correct length for β-strands. Turn propensity was high at frequent intervals, consistent with transmembrane β-strands. We propose that these proteins fold as porin-like 16-stranded antiparallel β-barrels. In water channels, from the size of molecules excluded, an extramembrane loop(s) would enter the pore and restrict it to a bottleneck with a width 4 Å ⩽w ⩽5 Å. A similar but more mobile loop(s) would act as gate and binding site for the facilitators of the MIP family.
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Abrami, L., Simon, M., Rousselet, G., Berthonaud, V., Buhler, J.M., Ripoche, P. 1994. Sequence and functional expression of an amphibian water channel, FA-CHIP: a new member of the CHIP family. Biochim. Biophys. Acta 1192:147–151
Agre, P., Preston, G.M., Smith, B.L., Jung, J.S., Raina, S., Moon, C., Guggino, W.B., Nielsen, S. 1993. Aquaporin CHIP: the archetypal molecular water channel. Am. J. Physiol. 265:F463-F476
Chepelinsky, A.B. 1994. The MIP transmembrane channel family. In: Handbook of membrane channels: molecular and cellular physiology. C. Peracchia, editor. pp. 413–432. Academic Press, San Diego, CA
Cowan, S.W., Rosenbusch, J.P. 1994. Folding pattern diversity of integral membrane proteins. Science 264:914–916
Cowan, S.W., Shirmer, T., Rummel, G., Steiert, M., Ghosh, R., Pauptit, R.A., Jansonius, J.N., Rosenbusch, J.P. 1992. Crystal structures explain functional properties of two E. coli porins. Nature 358:727–733
Eisenberg, D., Weiss, R.M., Terwilliger, T.C. 1984. The hydrophobic moment detects periodicity in protein hydrophobicity. Proc. Natl. Acad. Sci. USA 81:140–144
Fischbarg, J., Cheung, M., Czegledy, F., Li, J., Iserovich, P., Kuang, K., Hubbard, J., Garner, M, Rosen, O.M., Golde, D.W., Vera, J.C. 1993. Evidence that facilitative glucose transporters may fold as beta-barrels. Proc. Natl. Acad. Sci. USA 90:11658–11662
Fischbarg, J., Cheung, M., Li, J., Iserovich, P., Czegledy, F., Kuang, K., Garner, M. 1994. Are most transporters and channels beta barrels? Mol. Cell. Biochem. 140:147–162
Fushimi, K., Uchida, S., Hara, Y., Hirata, Y., Marumo, F., Sasaki, S. 1993. Cloning and expression of apical membrane water channel of rat kidney collecting tubule. Nature 361:549–552
Hasegawa, H., Zhang, R., Dohrman, A., Verkman, A.S. 1993. Tissue-specific expression of mRNA encoding rat kidney water channel CHIP28k by in situ hybridization. Am. J. Physiol. 264:C237-C245
Hays, R.M., Leaf, A. 1962. Studies on the movement of water through the isolated toad bladder and its modification by vasopressin. J. Gen. Physiol. 45:905–919
Jung, J.S., Preston, G.M., Smith, B.L., Guggino, W.B., Agre, P. 1994. Molecular structure of the water channel through aquaporin CHIP. The hourglass model. J. Biol. Chem. 269:14648–14654
Kyte, J., Doolittle, R.F. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105–132
Macey, R.I. 1984. Transport of water and urea in red blood cells. Am. J. Physiol. 246:C195-C203
Macey, R.I., Farmer, R.E.L. 1970. Inhibition of water and solute permeability in human red cells. Biochim. Biophys. Acta 211:104–106
Maurel, C., Reizer, J., Schroeder, J.I., Chrispeels, M.J. 1993. The vacuolar membrane protein g-TIP creates water specific channels in Xenopus oocytes. The EMBO Journal 12:2241–2247
Muramatsu, S., Mizuno, T. 1989. Nucleotide sequence of the region encompassing the glpKF operon and its upstream region containing a bent DNA sequence of Escherichia coli. Nucl. Acids Res. 17:4378
Nielsen, S., Smith, B.L., Christensen, E.I., Knepper, M.A., Agre, P. 1993. CHIP28 water channels are localized in constitutively water-permeable segments of the nephron. J. Cell Biol. 120:371–383
Parisi, M., Bourguet, J. 1983. The single-file hypothesis and the water channels induced by antidiuretic hormone. J. Membrane Biol. 71(3):189–193
Pisano, M.M., Chepelinsky, A.B. 1991. Genomic cloning, complete nucleotide sequence, and structure of the human gene encoding the major intrinsic protein (MIP) of the lens. Genomics 11:981–990
Preston, G.M., Agre, P. 1991. Isolation of the cDNA for erythrocyte integral membrane protein of 28 kilodaltons: Member of an ancient channel family. Proc. Natl. Acad. Sci. USA 88:11110–11114
Preston, G.M., Carroll, T.P., Guggino, W.B., Agre, P. 1992. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256:385–387
Preston, G.M., Jung, J.S., Guggino, W.B., Agre, P. 1993. The mercury-sensitive residue at cysteine 189 in the CHIP28 water channel. J. Biol. Chem. 268:17–20
Preston, G.M., Jung, J.S., Guggino, W.B., Agre, P. 1994. Membrane topology of aquaporin CHIP. Analysis of functional epitope-scanning mutants by vectorial proteolysis. J. Biol. Chem. 269:1668–1673
Prevelige, P., Fasman, G.D. 1989. In: Prediction of protein structure and the principles of protein conformation. G.D. Fasman, editor. pp. 391–416. Plenum, New York, London
Radding, W. 1991. Proposed partial beta-structures for lac permease and the Na+/H+ antiporter which use similar transport and H+ coupling mechanism. J. Theor. Biol. 150:239–249
Rao, Y., Jan, L.Y., Jan, Y.N. 1990. Similarity of the product of the Drosophila neurogenic gene big brain to transmembrane channel proteins. Nature 345:163–167
Rost, B., Sander, C. 1992. Jury returns on structure prediction. Nature 360:540
Sandal, N.N., Marcker, K.A. 1988. Soybean nodulin 26 is homologous to the major intrinsic protein of the bovine lens fiber membrane. Nucl. Acids Res. 16:9347
Solomon, A.K. 1968. Characterization of biological membranes by equivalent pores. J. Gen. Physiol. 51:335–364
Van Hoek, A.N., Verkman, A.S. 1992. Functional reconstitution of the isolated erythrocyte water channel CHIP28. J. Biol. Chem. 267:18267–18269
Van Hoek, A.N., Wiener, M., Bicknese, S., Miercke, L., Biwersi, J., Verkman, A.S. 1993. Secondary structure analysis of purified functional CHIP28 water channels by CD and FTIR spectroscopy. Biochemistry 32(44):11847–11856
Verkman, A.S. 1992. Water channels in cell membranes. Annu. Rev. Physiol. 54:97–108
Welte, W., Weiss, M.S., Nestel, U., Weckesser, J., Schiltz, E., Schulz, G.E. 1991. Prediction of the general structure of OmpF and PhoE from the sequence and structure of porin from Rhodobacter capsulatus. Orientation of porin in the membrane. Biochim. Biophys. Acta 1080:271–274
Whittembury, G., Echevarría, M., Gutierrez, A., Gonzalez, E. 1991. Contraluminal cell membrane water channels in PST exclude urea and acetamide but are formamide permeable. J. Am. Soc. Nephrol. 2:729
Zhang, R., Skach, W., Hasegawa, H., Van Hoek, A.N., Verkman, A.S. 1993a. Cloning, functional analysis and cell localization of a kidney proximal tubule water transporter homologous to CHIP28. J. Cell Biol. 120:359–369
Zhang, R., van-Hoek, A.N., Biwersi, J., Verkman, A.S. 1993b. A point mutation at cysteine 189 blocks the water permeability of rat kidney water channel CHIP28k. Biochemistry 32:2938–2941
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Fischbarg, J., Li, J., Cheung, M. et al. Predictive evidence for a porin-type β-barrel fold in CHIP28 and other members of the MIP family. A restricted-pore model common to water channels and facilitators. J. Membarin Biol. 143, 177–188 (1995). https://doi.org/10.1007/BF00233446
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DOI: https://doi.org/10.1007/BF00233446