Abstract
Among the most intriguing structures formed by inorganic polyphosphates (polyP) are their complexes with poly-(R)-3-hydroxybutyrates) (PHB) that form ion channels in lipid bilayers. All peptide and protein ion channels, as well as synthetic ion channels, are amphiphilic structures with an outer coat of non-polar residues and a lining of polar and charged residues (Urry 1985; Christensen et al. 1988; Nakano et al. 1990; Sansom 1991; Kobuke et al. 1992; Epand 1993; Fyles et al. 1993). These attributes are provided in a cooperative fashion by the two structurally distinct homopolymers, polyP and PHB. The polymeric anion, polyP, forms a ladder of cation binding sites that stretches across the bilayer, shielded from the hydrophobic environment by the amphiphilic solvating polyester, PHB. Complexes of polyP and PHB, located in the plasma membranes of diverse bacteria (Reusch and Sadoff 1983; Reusch et al. 1986, 1987), are the first nonproteinaceous, ion-selective channels discovered in biological cells. Their capacity to form voltage-activated, calcium-selective channels in planar lipid bilayers has been established (Reusch et al. 1995; Das et al. 1997). As yet, there is no direct evidence of their in vivo functions; however, a number of studies point to calcium involvement in important cellular functions in bacteria, such as chemotaxis (Matsushita et al. 1989; Tisa and Adler 1992) and cell division (Chang 1986; Smith 1995; Norris 1996). In addition, there is substantial evidence that polyP/PHB complexes may serve as calcium pumps and DNA channels. Here we will discuss the singular molecular characteristics of polyP and PHB that relate to their roles in ion transport, and consider how the two polymers act in synergy to form these interesting transmembrane ion channels.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Ahn K, Kornberg A (1990) Polyphoshate kinase from Escherichia coll. J Biol Chem 265: 11734–11739
Alvarez O, Benos D, Latorre R (1985) The study of ion channels in planar lipid bilayer membranes. J Electrophysiol Tech 12: 159–177
Ambudkar SV, Zlotnick EW, Rosen BP (1984) Calcium efflux from Escherichia colis : evidence for two systems. J Biol Chem 259: 6142–6146
Anderson AJ, Dawes EA (1990) Occurrence, metabolism, metabolic role, and industrial uses of bacterial polyhydroxyalkanoates. Microbiol Rev 54: 450–472
Antonov VF, Petrov VV, Molnar AA, Predvoditdelev DA, Ivanov AS (1980) The appearance of single-ion channels in unmodified lipid bilayer membranse at the phase transition temperature. Nature 283: 585–586
Armand MB (1987) Current state of PEO-based electrolyte. In: MacCallum JR, Vincent CA, (eds) Polymer electrolyte reviews 1. Elsevier, New York, pp 1–37
Barham PJ, Keller A, Otun EL, Holmes PA (1984) Crystallization and morphology of a bacterial thermoplastic: poly-3-hydroxybutyrate. M Mater Sci 19: 2781–2794
Bark K, Kampfer P, Sponner A, Dott W (1993) Polyphosphate-dependent enzymes in some coryneform bacteria isolated from sewage sludge. FEMS Microbiol Lett 107: 133–138
Brandi H, Aeberli B, Bachofen R, Schwegler I, Müller H-M, Bürger MH, Hoffmann T, Lengweiler UD, Seebach D (1995) Biodegradation of cyclic and substituted linear oligomers of poly(3hydroxybutyrate). Can J Microbiol 41: 180–186
Bruckner S, Meille AV, Malpezzi L, Cesaro A, Navarini L, Tombolini R (1988) The structure of poly(D-(-)-β-hydroxybutyrate). A refinement based on the Rietveld method. Macromolecules 21: 967–971
Bürger HM, Seebach D (1993) Cation transport across bulk liquid organic membranes with oligomers of (R)-3-hydroxybutanoic acid. Helv Chim Acta 76: 2570–2580
Castuma CE, Huang R, Kornberg A, Reusch RN (1995) Inorganic polyphosphates in the acquisition of competence. J Biol Chem 270: 12980–12983
Chang CF (1986) Electron probe analysis, X-ray mapping, and electron energy-loss spectroscopy of calcium, magnesium, and monovalent ions in log-phase and in dividing Escherichia coli B cells. J Bacteriol 167: 935–939
Christensen B, Fink J, Merrifield RB, Mauzerall D (1988) Channel-forming properties of cecropins and related model compounds incorporated into planar lipid membranes. Proc Nat! Acad Sci USA 85: 5072–5076
Corbridge DEC (1995) Phosphorus. An outline of its chemistry, biochemistry and technology. Stud Inorg Chem 20: 224–243
Cornibert J, Marchessault RH (1972) Physical properties of poly-ß-hydroxybutyrate. IV. Conformational analysis and crystal structure. J Mol Biol 71: 735–756
Cornibert J, Marchessault H (1975) Conformational isomorphism. A general 21 helical conformation for poly(ß-alkanoates). Macromolecules 8: 296–305
Crooke E, Akiyama M, Rao NN, Kornberg A (1994) Genetically altered levels of inorganic polyphosphate in Escherichia coll. J Biol Chem 269: 6290–6295
Dawes EA, Senior PJ (1973) The role and regulation of energy reserve polymers in microorganisms. Adv Microb Physiol 10: 135–206
Das S, Lengweiler UD, Seebach D, Reusch RN (1997) Proof for a nonproteinaceous calcium-selective channel by total synthesis from (R)-3-hydroxybutanoic acid and inorganic polyphosphate. Proc Natl Acad Sci USA 94: 9075–9079
Doi Y (1990) Microbial polyesters. VCH, New York
Dunham ET, Glynn IM (1961) Adenosinetriphosphate activity and the active movement of alkali metal ions. J Physiol 156: 274–293
Eisenman G, Horn R (1983) Ionic selectivity revisited: the role of kinetic and equilibrium processes in ion permeation through channels. J Membr Biol 76: 197–225
Epand RM (1993) The amphiatic helix. CRC Press, Ann Arbor, M, pp 222–246
Fettiplace D, Haydon A (1980) Water permeability of lipid membranes. Physiol Rev 60: 510–550
Fyles TM, James TD, Kaye KC (1993) Activities and modes of action of artificial ion channel mimics. J Am Chem Soc 115: 12315–12321
Gangola P, Rosen BP (1987) Maintenance of intracellular calcium in Escherichia coll. J Biol Chem 26: 12570–12574
Gray FM (1992) Solid polymer electrolytes. VCH, New York, pp 1–4
Griffin JB, Davidian NM, Penniall R (1965) Studies of phosphorus metabolism by isolated nuclei. J Biol Chem 240: 4427–4434
Hagiwara S, Byerly L (1981) Calcium channel. Annu Rev Neurosci 4: 69–125
Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557–580
Hanahan D, Bloom FR (1996) Mechanisms of DNA transformation. In: Neidhardt FC (ed) Escherichia coli and Salmonella : cellular and molecular Biology. ASM Press, Washington, DC, pp 2449–2459
Hess P, Tsien RW (1984) Mechanism of ion permeation through ion channels. Nature 309: 453–456
Hille B (1992) Ionic channels of excitable Membranes. Sinauer, Sunderland, MA
Holmes PA (1987) Biologically produced (R)-3-hydroxyalkanoate polymers and copolymers. In: Bassett DC (ed) Developments in crystalline polymers-2. Elsevier, New York, pp 1–65
Huang R, Reusch RN (1995) Genetic competence in Escherichia coli requires poly-(3hydroxybutyrate/calcium polyphosphate membrane complexes and certain divalent cations. J Bacteriol 177: 486–490
Huang R, Reusch RN (1996) Poly-(R)-3-hydroxybutyrate) is associated with specific protein in the cytoplasm and membranes of Escherichia coli. J Biol Chem 271: 22196–22202
Karr DB, Waters JK, Emerich DW (1983) Analysis of poly-f3-hydroxybutyrate in Rhizobium japonicum bacteroids by ion-exclusion high-pressure liquid chromatography and UV detec-tion. Appl Environ Microbiol 46: 1339–1344
Kobuke Y, Ueda K, Sokabe M (1992) Artificial non-peptide sinlge ion channels. J Am Chem Soc 114: 7618–7622
Kornberg A (1995) Inorganic polyphosphate: toward making a forgotten polymer unforgettable. J Bacteriol 177: 491–495
Kornberg A, Kornberg S, Simms E (1956) Metaphosphate synthesis by an enzyme from Escherichia coli. Biochim Biophys Acta 20: 215–227
Kosk-Kosicka D, Scaillet S, Inesi G (1986) The partial reactions in the catalytic cycle of the calcium-dependent adenosine triphosphatase purified from erythrocyte membranes. J Biol Chem 261: 3333–3338
Kulaev IS (1979) The biochemistry of inorganic polyphosphates. Wiley, New York, pp 1248
Kulaev IS, Vagabov VM (1983) Polyphosphate metabolism in micro-organisms. Adv Microb Physiol 24: 83–171
Kumble KD, Kornberg A (1995) Inorganic polyphosphate in mammalian cells and tissues. J Biol Chem 270: 5818–5822
Law JH, Slepecky RA (1961) Assay of poly-13-hydroxybutyric acid. J Bacteriol 82: 33–42
Lehn JM (1973) Design of organic complexing agents; strategies towards properties. Struct Bonding 16: 1–69
Lengweiler UD, Fritz MG, Seebach D (1996) Sythesis of monodisperse linear and cyclic oligo-mers of (R)-3-hydroxybutyric acid with 128 residues. Hely Chim Acta 79: 670–701
Lynn AR, Rosen BP (1987) Calcium transport in prokaryotes. In: Rosen BP, Silver S (eds) Ion transport in prokaryotes. Academic Press, New York, pp 181–201
MacCallum JR, Vincent CA (1987) Ion-molecule and ion-ion interactions. In: MacCallum JR, Vincent CA (eds) Polymer electrolyte reviews 1. Elsevier, New York, pp 23–37
Majling J, Hanic F (1980) Phase chemistry of condensed phosphates. Top Phosphorus Chem 10: 341–502
Mandel H, Higa A (1970) Calcium-dependent bacteriophage DNA infection. J Mol Biol 53: 159–162
Marchessault RH, Okamura K, Su CJ (1970) Physical properties of poly(3-hydroxybutyrate). II. Conformational aspects in solution. Macromolecules 3–735–740
Marsh D, Watts A, Knowles PF (1976) Evidence for phase boundary lipid. Permeability of tempo-choline into dimyristoylphosphatidylcholine vesicles at the phase transition. Biochemistry 15: 3570–3578
Martin RB (1990) Bioinorganic chemistry of magnesium. In: Sigel H, Sigel A (eds) Metal ions in biological systems vol 26. Dekker, New York pp 1–13
Matheja J, Degens ET (1971) Structural molecular Biology of phosphates. Fischer, Stuttgart, pp 78–90
Matsushita T, Hirata H, Kusaka I (1989) Calcium channels in bacteria. Ann N Y Acad Sci 560: 276–278
McCleskey EW, Almers W (1985) The Ca channel in skeletal muscle is a large pore. Proc Natl Acad Sci USA 82: 7149–7153
Miller C (1983) Integral membrane channels: studies in model membranes. Physiol Rev 63: 1209–1242
Müller HM, Seebach D (1994) Poly(hydroxyalkanoates): a fifth class of physiologically important organic biopolymers? Angew Chem 32: 477–502
Nakano A, Xie Q, Mallen JV, Echegoyen L, Gokel GW (1990) Synthesis of a membrane-insertable, sodium cation-conducting channel: kinetic analysis by dynamic 23Na NMR. J Am Chem Soc 112: 1287–1289
Niggli V, Penniston J, Carafoli E (1979) Purification of the (Ca2+-Mg2+)-ATPase from human erythrocyte membranes using a calmodulin affinity column. J Biol Chem 254: 9955–9958
Norris V, Grant S, Freestone P, Canvin J, Sheikh FN, Toth I, Triner M, Modha K, Norman R (1996) Calcium signalling in bacteria. J Bacteriol 178: 3677–3682
Overath P, Träuble H (1973) Phase transitions in cell membranes, and lipids of Escherichia coli. Detection by fluorescent probes, light scattering and dilatometry. Biochemistry 12: 2625–2634
Page WJ, von Tigerstrom M (1979) Optimal conditions for transformation of Azotobacter vinelandii. J Bacteriol 139: 1058–1061
Plattner DA, Brunner A, Dobler M, Müller HM, Petter W, Zbinden P, Seebach D (1993) Cyclic oligomers of (R)-3-hydroxybutanoic acid: preparation and structural aspects. Helv Chim Acta 76: 2004–2033
Reusch RN (1989) Poly-ß-hydroxybutyrate/calcium polyphosphate complexes in eukaryotic membranes. Proc Soc Exp Biol Med 191: 377–381
Reusch RN (1992) Biological complexes of poly-ß-hydroxybutyrate. FEMS Rev 103: 119–130
Reuch RN, Reusch WH (1993) Branched polyhydroxyalkanoate polymer salt compositions and method of preparation. US Patent no 5,266–422
Reusch RN, Sadoff HL (1983) D-(-)-poly-ß-hydroxybutyrate in membranes of genetically competent bacteria. J Bacteriol 156: 778–788
Reusch RN, Sadoff HL (1988) Putative structure and function of a poly-ß-hydroxybutyrate calcium polyphosphate channel in bacterial plasma membranes. Proc Natl Acad Sci USA
Reusch RN, Hiske TW, Sadoff HL (1986) Poly-ß-hydroxybutyrate membrane structure and its relationship to genetic transformability in Escherichia coli. J Bacteriol 168: 553–562
Reusch R, Hiske T, Sadoff H, Harris R, Beveridge T (1987) Cellular incorporation of poly-ßhydroxybutyrate into plasma membranes of Escherichia coli and Azotobacter vinelandii alters native membrane structure. Can J Microbiol 33: 435–444
Reusch RN, Sparrow AW, Gardiner J (1992) Transport of poly-ß-hydroxybutyrate in human plasma. Biochim Biophys Acta 1123: 33–40
Reusch RN, Huang R, Bramble LL (1995) Poly-3-hydroxybutyrate/polyphosphate complexes form voltage-activated/Ca2+ channels in the plasma membranes of Escherichia coli. Biophys J 69: 754–766
Reusch RN, Huang R, Kosk-Kosicka D (1997) Novel components and enzymatic activities of the human erythrocyte plasma membrane calcium pump. FEBS Lett 412: 592–596
Rosen BP, McClees JS (1974) Active transport of calcium in inverted membrane vesicles of Escherichia coli. Proc Natl Acad Sci USA 71: 5042–5046
Sansom MSP (1991) The biophysics of peptide models of ion channels. Prog Biophys Mol Biol 55: 139–151
Schatzmann HJ (1966) ATP-dependent Ca++-extrusion from human red cells. Experientia 22: 364–368
Seebach D, Brunner A, Bürger HM, Schneider J, Reusch RN (1994a) Isolation and 1H-NMR spectroscopic identification of poly-(R)-3-hydroxybutanoate) from prokaryotic and eukaryotic organisms. Eur J Biochem 224: 317–328
Seebach D, Bürger M, Müller HM, Lengweiler UD, Beck AK, Sykes KE, Barker PA, Barham PJ (1994b) Synthesis of linear oligomers of (R)-3-hydroxybutyrate and solid-state structural investigations by electron microscopy and x-ray scattering. Helv Chim Acta 77: 1099–1123
Seebach D, Brunner A, Bachmann BM, Hoffmann T, Kühnle FN, Lengweiler UD (1996a) Biopolymers and -oligomers of (R)-3-hydroxyalkanoic acids - contributions of synthetic organic chemists. Ernst Shering Res Found 28: 1–105
Seebach D, Brunner A, Bürger HM, Reusch RN, Bramble LL (1996b) Channel-forming activity of 3-hydroxybutanoic-acid oligomers in planar lipid bilayers. Helv Chim Acta 79: 507–517
Simon W, Morf WE, Meier PC (1973) Specificity for alkali and alkaline earth cations in mem-branes, Struct. Bonding 16: 113–160
Smith HO, Danner DB, Deich RA (1981) Genetic transformation. Annu Rev Biochem 50: 41–68
Smith RJ (1995) Calcium and bacteria. Adv Microb Physiol 37: 83–103
Sykes KE, McMaster TJ, Miles MJ, Barker PA, Barham PJ, Seebach D, Müller H-M, Lengweiler UD (1995) Direct imaging of the surfaces of poly-ß-hydroxybutyrate and hydroxybutyrate oligomers by atomic force microscopy. J Mater Sci 30: 623–627
Tanaka JC, Furman RE, Barchi RL (1986) Skeletal muscle sodium channels. Isolation and recon-stitution. In: Miller C (ed) Ion channel reconstitution. Plenum Press, New York, pp 277–305
Tinsley CR, Manjula BNK, Gotschlich EC (1993) Purification and characterization of polyphos-phate kinase from Neisseria meningitidis. Infect Immun 61: 3703–3710
Tisa LS, Adler J (1992) Calcium ions are involved in Escherichia colt chemotaxis. Proc Natl Acad Sci USA 89: 11804–11808
Träuble, H. Overath P (1973) Membrane structure of Escherichia colt. Biochim Biophys Acta 307: 491–512
Tsien RW, Hess P, McCleskey EW, Rosenberg RL (1987) Calcium channels: mechanisms of selectivity, permeation, and block. Annu Rev Biophys Biophys Chem 16: 265–290
Urry DW (1985) Chemical basis of ion transport specificity in biological membranes. Top Curr Chem 128: 175–218
Van Zutphen H, Merola AJ, Brierley GP, Cornwell DG (1972) The interaction of nonionic detergents with lipid bilayer membranes. Arch Biochem Biophys 152: 755–766
Watanabe M, Ogatu N (1987) In: MacCallum JR, Vincent CA (eds) Polymer electrolyte reviews 1. Elsevier, New York, pp 39–68
Watanabe M, Togo M, Sanui K, Ogatu N, Kobayashi T, Ohtaki Z (1984) Ionic conductivity of polymer complexes formed by poly(ß-propiolactone) and lithium perchlorate. Macromol Rev 17: 2908–2912
Welland EL, Stejny J, Halter A, Keller A (1989) Selective degradation of chain folded single crystals of poly)ß-hydroxybutyrate). Polym Commun 30: 302–304
Wilson PW, Knight SG (1952) Experiments in bacterial physiology. Burgess, Minneapolis, MJ
Wood HG, Clark JE (1988) Biological aspects of inorganic polyphosphates. Annu Rev Biochem 57: 235–260
Yamagata Y, Watanabe H, Saitoh M, Namba T (1991) Volcanic production of polyphosphates and its relevance to prebiotic evolution. Nature 352: 516–519
Yokouchi M, Chaitani Y, Tadokoror H, Teranishi K, Tani H (1973) Structural studies of polyesters: 5. Molecular and crystal structure of optically active and racemic poly(ß-hydroxybutyrate). Polymer 14: 267–272
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1999 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Reusch, R.N. (1999). Polyphosphate/Poly-(R)-3-Hydroxybutyrate) Ion Channels in Cell Membranes. In: Schröder, H.C., Müller, W.E.G. (eds) Inorganic Polyphosphates. Progress in Molecular and Subcellular Biology, vol 23. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-58444-2_8
Download citation
DOI: https://doi.org/10.1007/978-3-642-58444-2_8
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-63597-7
Online ISBN: 978-3-642-58444-2
eBook Packages: Springer Book Archive