a. PORE FORMATION IN PLANAR LIPID BILAYER MEMBRANES
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1 a. PORE FORMATION IN PLANAR LIPID BILAYER MEMBRANES Gianluigi Monticelli Istituto di Fisiologia generale e Chimica biologica, Università degli Studi, Via Saldini 50, Milano - ITALY INTRODUCTION Porins constitute a class of proteins located in the outer membranes of mitochondria and of gram-negative bacteria. These proteins form large water filled pores through the hydrophobic core of the outer membrane (1-4). This channel system acts as a molecular filter with a defined exclusion limit for hydrophilic substances (3, 5, 6). Sugars and other hydrophilic solutes up to a molecular weight of (7-10) permeate the outer membrane of gram-negative bacteria, such as Escherichia coli, Salmonella thyphimurium, Proteus mirabilis. In some cases it seems that porin forms solute-specific channels as protein P of Pseudomonas aeruginosa (11) and maltoporin of Escherichia coli (12, 13). The outer mitochondrial membrane is freely permeable to various small solutes, too, but not to molecules of large weight (14-18). Porin, this pore forming protein, was identified in the outer mitochondrial membrane of a variety of eukariotic cells (17, 19-24). It was named mitochondrial porin in analogy to the bacterial porins and it is also known as voltage-dependent anion-selective channel (VDAC) (19, 20). Mitochondrial porins are polypeptides with molecular weights between and (18, 21-26). In gram-negative bacteria proteins giving this passive permeability were variously called: protein I (27), protein 1 (28), matrix protein (29) and porins (1). These proteins range in molecular weight from to and common features were determined examining more than 40 different porins (30). Mitochondrial porin formed pores share some similarities with the bacterial porins located in the bacterial outer membranes (24). The formed diffusion pores have a diameter of nm in bacteria and nm in mitochondria approximatively (23, 24, 31). It has been proposed that porins from bacteria usually exist in the membrane as trimers and the pore appears to be formed by β-sheet rather than α-helices (32); moreover it has been demonstrated that three channels on the outer surface of the cell merge into a single channel at the periplasmic face (33).
2 The outer mitochondrial membrane contains only one type of porin (21) and the pore permeability seems to be controlled by a transmembrane potential or an intrinsic membrane potential; many studied porins are voltage-dependent and switch to substates when transmembrane potential is higher than mv (19-24). Open pores present an higher permeability and a different ionic selectivity than the substates (19, 23, 24, 34). Pore forming properties can be studied in reconstitution experiments with planar lipid bilayers and liposomes. Incorporation of lipid components from bacteria outer membrane into phospholipid vesicles rendered the vesicle membrane permeable to small sugar molecules (1, 35, 36) and it has been demonstrated that incorporation of the matrix protein from Escherichia coli into phospholipid/lipopolysaccharide vesicles induced permeability to hidrophilic solutes up to molecular weight of about 550 (1). Planar bilayers which separate two well defined aqueous phases offer the possibility of directly measuring electrical parameters as well as to follow the kinetics of porin incorporation. Many papers have been published on the determination of ion permeability through the channels made of porins from outer membrane of bacteria (31, 37-40) and of mitochondria (18-21, 23, 41-44). PORIN CHANNELS The addition of small amounts of porin to the solutions bathing a lipid bilayer membrane having small surface area allowed the resolution of step increases of conductance. The average conductance increment, as determined by measuring a large number of events, for different lipid membranes and porins are reported in Table I with the reference source. TABLE I Salt c [M] Λ [ns] Λ/λ [Å] λ [ms/cm] r=l/λ [Ωcm] d [nm] Ref. n. Egg lecithin/n-decane (ph : V m =50 mv: t=25 ºC) Pseudomonas aeruginosa protein F: l nm NaC KC Asolectin (L-α-phosphatidylcholine)/n-decane (ph 6.0: V m =5 mv: t=25 ºC) Rat liver porin l µg/ml KC NaC
3 LiC RbC MgC K 2 S Tris + Hepes - (ph 8.0) N(C 2 H 5 ) + Hepes Diphytanoylphosphatidylcholine/n-decane (ph : V m =10 mv: t=25 ºC) Rat brain porin 1.2 ng/ml KC NaC RbC CH 3 COOK LiC MgC Na 2 SO Tris-HC Salt c [M] Λ [ns] Λ/λ [Å] λ [ms/cm] r=l/λ [Ωcm] d [nm] Ref. n. Oxidized cholesterol/n-decane (ph : V m =50 mv) E. coli porin 0.5 ng/ml KC NaC RbC LiC CsC NH 4 C MgC CaC BaC K 2 S MgS Na + Hepes - (ph 9.0) Tris + C Tris + Hepes - (ph 8.0) Glucosamine + C1 - (ph ) N(CH 3 ) + 4 C N(CH 3 ) + 4 Hepes - (ph 8.5) N(C 2 H 5 ) + Hepes Salmonella typhimurium SH5551 (40K) 1 pm trimers LiC NaC
4 KC NH 4 C RbC CsC MgC CaC K 2 S MgS Na + Hepes - (ph 9.0) Tris + C Tris + Hepes - (ph 8.0) Glucosamine + C1 - (ph ) N(CH 3 ) + 4 C N(CH 3 ) + 4 Hepes - (ph 8.5) N(C 2 H 5 ) + Hepes Pseudomonas aeruginosa protein F 1 nm NaC KC MgC CaC K 2 S Na + Hepes - (ph 9.0) Tris + C Tris + Hepes- (ph 8.0) N(CH 3 ) + 4 C N(CH 3 ) + 4 Hepes - (ph 8.5) N(C 2 H 5 ) + Hepes In this table in addition to the specific conductance (Λ), the specific conductance λ of the corresponding aqueous solution, the ratio Λ/λ and the effective pore diameter d are given. The pore diameter d was calculated assuming a membrane tickness l=7.5 nm and considering that the pore is a cylinder with a circular cross section and is filled with an aqueous solution of the same conductance as the external bulk phase. With these assumptions it is: Λ = λπr 2 /l and the pore diameter (2r) can be calculated. The analysis of Table I shows that: 1) pores of different diameter can be formed depending on the porin origin and on the bilayer composition; 2) pore conductance is a
5 linear function of the specific conductance of the aqueous phase; 3) large organic cations and anions are able to permeate porin channels practically without interactions with the pore walls. SIMPLE GEOMETRICAL CONSIDERATIONS From a geometrical point of view the pore formation into a planar lipid bilayer membrane can be represented as schematized in Fig. 1. After addition of porin to bulk phases, as time passes, there is an increase of the number of pores. If S p and S o are the single pore area and the total area occupied by lipids at t=0 respectively, the membrane lipid area at time t, when n(t) aqueous channels have been formed, is: S(t) = S o - n(t) S p - 2
6 This evolution of the membrane incorporating protein channels can be schematized electrically as in Fig. 2. Before porin addition the BLM equivalent circuit is constituted by a parallel combination of the resistance R mo and capacitance C mo. As pores are formed the surface area of membrane lipid part decreases so that the relative resistance and capacitance are time dependent: R lm (t) and C m (t). Single channel resistances (R sc ) are connected in parallel constituting pathways for ion transport. At time t the equivalent electrical circuit can be semplified as in Fig. 3 where R lm [n(t)] is the resistance of lipid part of the membrane, R p [n(t)] is the total electrical resistance of pores and C m [n(t)] is the membrane capacitance. In this picture pores are characterized by the conductance only and moreover it has been neglected the thickness increase of the lipid part because of the aqueous holes (pores) into the membrane. Increasing the number of channels R p [n(t)] decreases as R sc /n(t). Due to the pore formation the resistance of the membrane lipid part increases according to: R lm (t) = R mo {1/[1-S p n(t)/s o ]} For the same reason the capacitance of membrane lipid part decreases following C m (t) = C mo [1-S p n(t)/s o ] and the capacitative reactance X c = 1/ω C m (t) (ω = 2πf, where f is the frequency) increases with the number of pores. With this simple picture of the system and with the restrictions introduced by the simplifying hypothesis (constant tickness during porin incorporation and homogeneity
7 of the lipid film) it is possible to calculate the different electrical characteristics of the membrane if it is known the resistance and the diameter of a single channel. From the experimental point of view one problem can be constituted by the membrane capacitance as it has been well shown by White and Thompson (45, 46). In the normalization of capacitance with respect to area the bilayer film area must be precisely determined. Knowing the kinetics of pore formation, n(t), the dependence of calculated parameters on the number of formed pores can be transformed in the dependence on time. On the other hand current measurements during channel formation give informations on the number of protein complex functionning as pores. ACKNOWLEDGEMENTS I wish to thank Prof.s E. Gallucci and S. Micelli as well as Dr. J. Hladyszowski for the useful discussions and criticism. Work supported in part by a MPI 60% grant. REFERENCES 1) NAKAE T. - Biochem. Biophys. Res. Commun. 71: (1976). 2) NAKAE T. and ISHII J. - J. Bacteriol. 133: (1978). 3) NIKAIDO H. - In Bacterial outer Membranes: Biogenesis and Functions (Inouye M. ed.) , Wiley-Interscience, New York (1979). 4) HANCOCK R.E.W., DECAD G.M. and NIKAIDO H. - Biochim. Biophys. Acta 554: (1979). 5) DECAD G.M. and NIKAIDO H. - J. Bacteriol. 128: (1976). 6) HANCOCK R.E.W. and NIKAIDO H. - J. Bacteriol. 136: (1978). 7) NAKAE T. and NIKAIDO H. - J. Biol. Chem. 250: (1975). 8) NIKAIDO H. - Biochim. Biophys. Acta 433: (1976). 9) NIKAIDO H., SONG S.A., SHALTIEL L. and NURMINEN M. - Biochem. Biophys. Res. Commun. 76: (1977). 10) LUTKENHAUS J.F. - J. Bacteriol. 131: (1977). 11) BENZ R., GIMPLE M., POOLE K. and HANCOCK R.E.W. - Biochim. Biophys. Acta 730: (1983). 12) LUCKEY M. and NIKAIDO H. - Biochem. Biophys. Res. Commun. 93: (1980). 13) LUCKEY M. and NIKAIDO H. - Proc. Natl. Acad. Sci. U.S.A. 77: (1980). 14) WERKHEISER W.C. and BARTLEY W. - Biochem. J. 66: (1957). 15) O'BRIEN R.L. and BRIERLY G. - J. Biol. Chem. 240: (1965). 16) PFAFF E., KLINGENBERG M., RITT E. and VOGELL W. - Eur. J. Biochem. 5: (1968). 17) WOJTCZAK L. and ZALUSKA H. - Biochim. Biophys. Acta 193: (1969). 18) DE PINTO V., TOMMASINO M., BENZ R. and PALMIERI F. - Biochim. Biophys. Acta 813: (1985). 19) SCHEIN S.J., COLOMBINI M. and FINKELSTEIN A. - J. Membrane Biol. 30: (1976).
8 20) COLOMBINI M. - Nature (London) 279: (1979). 21) ROOS N., BENZ R. and BRDICZKA D. - Biochim. Biophys. Acta 686: (1982). 22) FREITAG H., NEUPERT W. and BENZ R. - Europ. J. Biochem. 123: (1982). 23) BENZ R., LUDWIG O., DE PINTO V. and PALMIERI F. - In Achievements and Perspectives of Mitochondrial Research, 1: Bioenergetics (Quagliariello E. et al. eds.) , Elsevier, Amsterdam (1985). 24) BENZ R. - CRC Crit. Rev. Biochem. 19: (1985). 25) ZALMAN L.S., NIKAIDO H. and KAGAWA Y. - J. Biol. Chem, 255: (1980). 26) COLOMBINI M. - J. Membrane Biol. 74: (1983). 27) HENNING V., HOHN B. and SOUNTAG J. - Eur. J. Biochem. 39: (1973). 28) SCHNAITMAN C.A. - J. Bacteriol. 118: (1974). 29) ROSENBUSCH J.P. - J. Biol. Chem. 249: (1974). 30) BAINES A.J. and BENNETT V. - Nature (London) 315: (1985). 31) BENZ R. and HANCOCK R.E.W. - Biochim. Biophys. Acta 646: (1981). 32) VOGEL H. and JAHNIG F. - J. Mol. Biol. 190: (1986). 33) ENGEL A., MASSALSKI A., SCHINDLER H., DORSET D.L. and ROSENBUSCH J.P. - Nature (London) 317: (1985). 34) BRDICZKA D., KNOLL G., RIESINGER I., WEILER U., KLUG G., BENZ R. and KRAUSE J. - In Myocardial and Skeletal Muscle Bioenergetics (Brautbar N. ed.) 55-70, Plenum Press, New York (1986). 35) NAKAE T. - Biochem. Biophys. Res. Commun. 64: (1975). 36) NAKAE T. - J. Biol. Chem. 251: (1976). 37) BENZ R., JANKO K., BOOS W. and LAUGER P. - Biochim. Biophys. Acta 511: (1978). 38) BENZ R., JANKO K. and LAUGER P. - Biochim. Biophys. Acta 551: (1979). 39) BENZ R., ISHII J. and NAKAE T. - J. Membrane Biol. 56: (1980). 40) BENZ R. - In Ion Channel Reconstitution (Miller C. ed.) , Plenum Press, New York (1986). 41) LUDWIG O., DE PINTO V., PALMIERI F. and BENZ R. - Biochim. Biophys. Acta 860: (1986). 42) DE PINTO V., LUDWIG O., KRAUSE J., BENZ R. and PALMIERI F. - Biochim. Biophys. Acta 894: (1987). 43) HARRIS A.L., WALTER A. and ZIMMERBERG J. - J. Membrane Biol. 109: (1989). 44) DE PINTO V., BENZ R. and PALMIERI F. - Eur. J. Biochem. 183: (1989). 45) WHITE S.H. - Biophys. J. 10: (1970). 46) WHITE S.H. and THOMPSON T.E. - Biochim. Biophys. Acta 323: 7-22 (1973). Proc. X School on Biophysics of Membrane Transport, Szczyrx (Poland) 1990, 1:
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