Proton in the well and through the desolvation barrier

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1757, Issue 5-6, 2006, Pages 415-427

  Mulkidjanian, Armen Y ^a,b  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

Bacterial flagellum; Chemiosmotic theory; Cytochrome bc1 complex; FOF1 type ATP synthase; Membrane transport; Proton transfer; Rhodobacter capsulatus; Solvation energy

Indexed keywords

PROTON; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; UBIQUINOL CYTOCHROME C REDUCTASE;

ENERGY; FORCE; NONHUMAN; PRIORITY JOURNAL; PROTON TRANSPORT; REVIEW;

BIOLOGICAL TRANSPORT; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX III; HYDROGEN-ION CONCENTRATION; INTRACELLULAR MEMBRANES; MEMBRANE POTENTIALS; MODELS, MOLECULAR; PROTON PUMPS; PROTON-MOTIVE FORCE; PROTON-TRANSLOCATING ATPASES; PROTONS; RHODOBACTER CAPSULATUS; WATER;

EID: 33745593970     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2006.04.023     Document Type: Review

References (142)

1. Carroll L. Alice's Adventures in Wonderland (1865), Macmillan, London
2. Mitchell P. Coupling of photophosphorylation to electron and hydrogen transfer by a chemiosmotic type of mechanism. Nature 191 (1961) 144-148
3. Mitchell P. Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Physiol. Rev. 41 (1966) 445-502
4. Mitchell P. Epilogue: from energetic abstraction to biochemical mechanism. Symp. Soc. Gen. Microbiol. 27 (1977) 383-423
5. Cramer W.A., and Knaff D.B. Energy Transduction in Biological Membranes: A Textbook of Bioenergetics (1991), Springer, New York
6. + is not unique as a coupling ion. Eur. J. Biochem. 151 (1985) 199-208
7. Hase C.C., Fedorova N.D., Galperin M.Y., and Dibrov P.A. Sodium ion cycle in bacterial pathogens: evidence from cross-genome comparisons. Microbiol. Mol. Biol. Rev. 65 (2001) 353-370
8. Cherepanov D.A., Feniouk B.A., Junge W., and Mulkidjanian A.Y. Low dielectric permittivity of water at the membrane interface: effect on the energy coupling mechanism in biological membranes. Biophys. J. 85 (2003) 1307-1316
9. Cherepanov D.A., Junge W., and Mulkidjanian A.Y. Proton transfer dynamics at the membrane/water interface: dependence on the fixed and mobile pH buffers, on the size and form of membrane particles, and on the interfacial potential barrier. Biophys. J. 86 (2004) 665-680
10. A.Y. Mulkidjanian, J. Heberle, D.A. Cherepanov, Protons @ interfaces: Implications for biological energy conversion, Biochim. Biophys. Acta (in press) doi:10.1016/j.bbabio.2006.02.015.
11. A.Y. Mulkidjanian, D.A. Cherepanov, Probing biological interfaces by tracing proton passage across them, Photochem. Photobiol. Sci. (in press) doi:10.1039/b516443e.
12. Carroll L. Through the Looking Glass (1872), Macmillan, London
13. Mitchell P. Chemiosmotic Coupling and Energy Transduction (1968), Glynn Research, Bodmin
14. Artsatbanov V.I., Konstantinov A.A., and Skulachev V.P. Involvement of intramitochondrial protons in redox reactions of cytochrome a. FEBS Lett. 78 (1978) 180-185
15. Glagolev A.N., and Skulachev V.P. The proton pump is a molecular engine of motile bacteria. Nature 272 (1978) 280-282
16. Skulachev V.P. The Energetics of Biological Membranes (1989), Nauka, Moscow
17. + release and uptake, and electric events in bacteriorhodopsin. FEBS Lett. 178 (1984) 331-336
18. Junge W., Lill H., and Engelbrecht S. ATP synthase: an electrochemical transducer with rotatory mechanics. Trends Biochem. Sci. 22 (1997) 420-423
19. Wikstrom M., Verkhovsky M.I., and Hummer G. Water-gated mechanism of proton translocation by cytochrome c oxidase. Biochim. Biophys. Acta 1604 (2003) 61-65
20. Faxen K., Gilderson G., Adelroth P., and Brzezinski P. A mechanistic principle for proton pumping by cytochrome c oxidase. Nature 437 (2005) 286-289
21. Lanyi J.K. Proton transfers in the bacteriorhodopsin photocycle. Biochim. Biophys. Acta (2005) 10.1016/j.bbabio.2005.11.003
22. Ohnishi T., and Salerno J.C. Conformation-driven and semiquinone-gated proton-pump mechanism in the NADH-ubiquinone oxidoreductase (complex I). FEBS Lett. 579 (2005) 4555-4561
23. Oster G., and Wang H. Rotary protein motors. Trends Cell Biol. 13 (2003) 114-121
24. Hofacker I., and Schulten K. Oxygen and proton pathways in cytochrome c oxidase. Proteins 30 (1998) 100-107
25. 1 complex from the yeast Saccharomyces cerevisiae co-crystallized with an antibody Fv fragment. Struct. Fold. Des. 8 (2000) 669-684
26. Svensson-Ek M., Abramson J., Larsson G., Tornroth S., Brzezinski P., and Iwata S. The X-ray crystal structures of wild-type and EQ(I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides. J. Mol. Biol. 321 (2002) 329-339
27. Born M. Volumen und Hydratationswärme der Ionen. Z. Phys. 1 (1920) 45-48
28. Warshel A., and Russell S.T. Calculations of electrostatic interactions in biological systems and in solutions. Q. Rev. Biophys. 17 (1984) 283-422
29. Parsegian A.V. Energy of an ion crossing a low dielectric membrane: solutions to four relevant electrostatic problems. Nature 221 (1969) 844-846
30. Mulkidjanian A.Y., Cherepanov D.A., Haumann M., and Junge W. Photosystem II of green plants: topology of core pigments and redox cofactors as inferred from electrochromic difference spectra. Biochemistry 35 (1996) 3093-3107
31. Burykin A., and Warshel A. What really prevents proton transport through aquaporin? Charge self-energy versus proton wire proposals. Biophys. J. 85 (2003) 3696-3706
32. de Groot B.L., and Grubmuller H. The dynamics and energetics of water permeation and proton exclusion in aquaporins. Curr. Opin. Struct. Biol. 15 (2005) 176-183
33. Krishtalik L.I. Activation energy for charge transfer reactions in membranes. Proton-translocating proteins. J. Electroanal. Chem. 204 (1986) 245-255
34. Burykin A., Kato M., and Warshel A. Exploring the origin of the ion selectivity of the KcsA potassium channel. Proteins 52 (2003) 412-426
35. Jensen M.O., Tajkhorshid E., and Schulten K. Electrostatic tuning of permeation and selectivity in aquaporin water channels. Biophys J. 85 (2003) 2884-2899
36. Braun-Sand S., Burykin A., Chu Z.T., and Warshel A. Realistic simulations of proton transport along the gramicidin channel: demonstrating the importance of solvation effects. J. Phys. Chem. B 109 (2005) 583-592
37. Koshland D.E. Application of a theory of enzyme specificity to protein synthesis. Proc. Natl. Acad. Sci. U. S. A. 44 (1958) 98-104
38. Heberle J. Proton transfer reactions across bacteriorhodopsin and along the membrane. Biochim. Biophys. Acta 1458 (2000) 135-147
39. Cherepanov D.A., Krishtalik L.I., and Mulkidjanian A.Y. Photosynthetic electron transfer controlled by protein relaxation: analysis by Langevin stochastic approach. Biophys. J. 80 (2001) 1033-1049
40. Boyer P.D. The ATP synthase-a splendid molecular machine. Annu. Rev. Biochem. 66 (1997) 717-749
41. O subunits. Biochim. Biophys. Acta 1458 (2000) 364-373
42. 1-ATPase with nucleotide bound to all three catalytic sites: implications for the mechanism of rotary catalysis. Cell 106 (2001) 331-341
43. 1-ATP synthase. Biochim. Biophys. Acta 1553 (2002) 188-211
44. O motor of the sodium ATPase. Biophys. J. 87 (2004) 2148-2163
45. O symmetry mismatch is not obligatory. EMBO Rep. 6 (2005) 1040-1044
46. 1 ATPases. Rolling well and turnstile hypothesis. FEBS Lett. 182 (1985) 1-7
47. Lightowlers R.N., Howitt S.M., Hatch L., Gibson F., and Cox G.B. The proton pore in the Escherichia coli F0F1-ATPase: a requirement for arginine at position 210 of the a-subunit. Biochim. Biophys. Acta 894 (1987) 399-406
48. 1 ATPase of Escherichia coli. Mutagenic analysis of the a subunit. J. Biol. Chem. 264 (1989) 3292-3300
49. 1 ATP synthase: structure and role in transmembrane energy transduction. Biochim. Biophys. Acta 1101 (1992) 240-243
50. 1 ATP synthases suggested by double mutants of the a subunit. J. Biol. Chem. 269 (1994) 30364-30369
51. Dimroth P., Kaim G., and Matthey U. The motor of the ATP synthase. Biochim. Biophys. Acta 1365 (1998) 87-92
52. Manson M.D., Tedesco P., Berg H.C., Harold F.M., and Van der Drift C. A protonmotive force drives bacterial flagella. Proc. Natl. Acad. Sci. U. S. A. 74 (1977) 3060-3064
53. Graber P., and Witt H.T. Relations between the electrical potential, pH gradient, proton flux and phosphorylation in the photosynthetic membrane. Biochim. Biophys. Acta 423 (1976) 141-163
54. Feniouk B.A., Kozlova M.A., Knorre D.A., Cherepanov D.A., Mulkidjanian A.Y., and Junge W. The proton driven rotor of ATP synthase: ohmic conductance (10 fS), and absence of voltage gating. Biophys. J. 86 (2004) 4094-4109
55. Elston T., Wang H., and Oster G. Energy transduction in ATP synthase. Nature 391 (1998) 510-513
56. Cherepanov D.A., Mulkidjanian A.Y., and Junge W. Transient accumulation of elastic energy in proton translocating ATP synthase. FEBS Lett. 449 (1999) 1-6
57. Wraight C.A., Cogdell R.J., and Chance B. Ion transport and electrochemical gradients in photosynthetic bacteria. In: Clayton R.K., and Sistrom W.R. (Eds). The Photosynthetic Bacteria (1978), Academic Press, New York 471-511
58. Junge W., and Jackson J.B. The development of electrochemical potential gradients across photosynthetic membranes. In: Govindjee (Ed). Photosynthesis vol. 1 (1982), Academic Press, New York 589-646
59. Junge W. Complete tracking of transient proton flow through active chloroplast ATP synthase. Proc. Natl. Acad. Sci. U. S. A. 84 (1987) 7084-7088
60. 1 under the ATP synthesis and slip conditions. FEBS Lett. 445 (1999) 409-414
61. 1-ATP synthase is absent from about half of chromatophores. Biochim. Biophys. Acta 1506 (2001) 189-203
62. 1-ATP synthase each. Biophys. J. 82 (2002) 1115-1122
63. Althoff G., Lill H., and Junge W. Proton channel of the chloroplast ATP synthase, CFo: its time-averaged single-channel conductance as function of pH, temperature, isotopic and ionic medium composition. J. Membr. Biol. 108 (1989) 263-271
64. Hatch L.P., Cox G.B., and Howitt S.M. The essential arginine residue at position 210 in the a subunit of the Escherichia coli ATP synthase can be transferred to position 252 with partial retention of activity. J. Biol. Chem. 270 (1995) 29407-29412
65. 1 ATP synthase: aqueous access channels and helix rotations at the a-c interface. Biochim. Biophys. Acta 1555 (2002) 29-36
66. Dmitriev O.Y., Altendorf K., and Fillingame R.H. Subunit a of the E. coli ATP synthase: reconstitution and high resolution NMR with protein purified in a mixed polarity solvent. FEBS Lett. 556 (2004) 35-38
67. O sector of ATP synthase. Biophys. J. 86 (2004) 1332-1344
68. +-ATPase from Ilyobacter tartaricus. Science 308 (2005) 659-662
69. Angevine C.M., and Fillingame R.H. Aqueous access channels in subunit a of rotary ATP synthase. J. Biol. Chem. 278 (2003) 6066-6074
70. Angevine C.M., Herold K.A., and Fillingame R.H. Aqueous access pathways in subunit a of rotary ATP synthase extend to both sides of the membrane. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 13179-13183
71. 1-ATPase in Escherichia coli. J. Biol. Chem. 263 (1988) 6606-6612
72. 1-ATP synthase. J. Biol. Chem. 272 (1997) 32635-32641
73. Hatch L.P., Cox G.B., and Howitt S.M. Glutamate residues at positions 219 and 252 in the a-subunit of the Escherichia coli ATP synthase are not functionally equivalent. Biochim. Biophys. Acta 1363 (1998) 217-223
74. Turina P., and Melandri B.A. A point mutation in the ATP synthase of Rhodobacter capsulatus results in differential contributions of ΔpH and Δψ in driving the ATP synthesis reaction. Eur. J. Biochem. 269 (2002) 1984-1992
75. Breton J., and Nabedryk E. Proton uptake upon quinone reduction in bacterial reaction centers: IR signature and possible participation of a highly polarizable hydrogen bond network. PR 55 (1998) 301-307
76. le Coutre J., Tittor J., Oesterhelt D., and Gerwert K. Experimental evidence for hydrogen-bonded network proton transfer in bacteriorhodopsin shown by Fourier-transform infrared spectroscopy using azide as catalyst. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 4962-4966
77. Garczarek F., Brown L.S., Lanyi J.K., and Gerwert K. Proton binding within a membrane protein by a protonated water cluster. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 3633-3638
78. Zundel G. Hydrogen bonds with large proton polarizability and proton transfer processes in electrochemistry and biology. Adv. Chem. Phys. 111 (2000) 1-217
79. Spassov V.Z., Luecke H., Gerwert K., and Bashford D. pKa calculations suggest storage of an excess proton in a hydrogen-bonded water network in bacteriorhodopsin. J. Mol. Biol. 312 (2001) 203-219
80. 1 ATP synthase. J. Biol. Chem. 273 (1998) 16241-16247
81. Rastogi V.K., and Girvin M.E. Structural changes linked to proton translocation by subunit c of the ATP synthase. Nature 402 (1999) 263-268
82. Fillingame R.H., Angevine C.M., and Dmitriev O.Y. Mechanics of coupling proton movements to c-ring rotation in ATP synthase. FEBS Lett. 555 (2003) 29-34
83. 1-ATP synthase of Escherichia coli defined by disulfide cross-linking. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 6607-6612
84. Fillingame R.H. The proton-translocating pumps of oxidative phosphorylation. Annu. Rev. Biochem. 49 (1980) 1079-1113
85. Boyer P.D. Bioenergetic coupling to protonmotive force: should we be considering hydronium ion coordination and not group protonation?. Trends Biochem. Sci. 13 (1988) 5-7
86. Blair D.F. Flagellar movement driven by proton translocation. FEBS Lett. 545 (2003) 86-95
87. Trumpower B.L., and Gennis R.B. Energy transduction by cytochrome complexes in mitochondrial and bacterial respiration: the enzymology of coupling electron transfer reactions to transmembrane proton translocation. Ann. Rev. Biochem. 63 (1994) 675-716
88. Berry E.A., Guergova-Kuras M., Huang L.S., and Crofts A.R. Structure and function of cytochrome bc complexes. Annu. Rev. Biochem. 69 (2000) 1005-1075
89. 1: comparison with its mitochondrial and chloroplast counterparts. Photosynth. Res. 81 (2004) 251-275
90. Mitchell P. Possible molecular mechanisms of the protonmotive function of cytochrome systems. J. Theor. Biol. 62 (1976) 327-367
91. 1 complex. J. Biol. Chem. 265 (1990) 11409-11412
92. 1. Nature 392 (1998) 677-684
93. 1 complex from bovine heart. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 8026-8033
94. 1 complex of Rhodobacter capsulatus: ubiquinol oxidation in a dimeric Q-cycle?. FEBS Lett. 431 (1998) 291-296
95. 1 complex. FEBS Lett. 545 (2003) 39-46
96. Osyczka A., Moser C.C., Daldal F., and Dutton P.L. Reversible redox energy coupling in electron transfer chains. Nature 427 (2004) 607-612
97. Rich P.R. The quinone chemistry of bc complexes. Biochim. Biophys. Acta 1658 (2004) 165-171
98. Mulkidjanian A.Y. Ubiquinol oxidation in the cytochrome bc complex: reaction mechanism and prevention of short-circuiting. Biochim. Biophys. Acta 1709 (2005) 5-34
99. 1 complex from bovine heart mitochondria. Science 277 (1997) 60-66
100. 1 complex. Science 281 (1998) 64-71
101. 1 with bound substrate and inhibitors at the Qi site. Biochemistry 42 (2003) 9067-9080
102. 1 complex with a hydroxyquinone anion Qo site inhibitor bound. J. Biol. Chem. 278 (2003) 31303-31311
103. 1 complex. J. Mol. Biol. 341 (2004) 281-302
104. Brugna M., Rodgers S., Schricker A., Montoya G., Kazmeier M., Nitschke W., and Sinning I. A spectroscopic method for observing the domain movement of the Rieske iron-sulfur protein. Proc. Acad. Sci. U. S. A. 97 (2000) 2069-2074
105. 1-complex is strongly electrogenic. FEBS Lett. 353 (1994) 189-193
106. 1 and the voltage generation. Biochim. Biophys. Acta-Bioenerg. 1553 (2002) 177-182
107. Klishin S.S., and Mulkidjanian A.Y. Proton transfer paths at the quinol oxidizing site of the Rb. capsulatus cytochrome bc complex. In: van der Est A., and Bruce D. (Eds). Photosynthesis: Fundamental Aspects to Global Perspectives vol. 1 (2005), Allen Press Inc., Lawrence/Montreal 260-262
108. 1 Complex of Rhodobacter capsulatus, PhD thesis, Lomonosov University, Moscow, 2005.
109. Skulachev V.P., Chistyakov V.V., Jasaitis A.A., and Smirnova E.G. Inhibition of the respiratory chain by zinc ions. Biochem. Biophys. Res. Commun. 26 (1967) 1-6
110. 1 complex by blocking a protonatable group. J. Biol. Chem. 270 (1995) 25001-25006
111. 1 complex. Biochim. Biophys. Acta 1459 (2000) 440-448
112. 1 complexes of phototrophic bacteria, Photochem. Photobiol. Sci. (submitted for publication).
113. Wikstrom M.K. The different cytochrome b components in the respiratory chain of animal mitochondria and their role in electron transport and energy conservation. Biochim. Biophys. Acta 301 (1973) 155-193
114. Wikstrom M., Krab K., and Saraste M. Proton-translocating cytochrome complexes. Annu. Rev. Biochem. 50 (1981) 623-655
115. King T.E., Yu C.A., Yu L., and Chiang Y.L. An examination of the components, sequence, mechanisms and their incertainties involved in mitochondrial electron transport from succinate to cytochrome c. In: Quagliariello E., Papa S., Palmieri F., Slater E.C., and Siliprandi N. (Eds). Electron Transfer Chain and Oxidative Phosphorylation (1975), North-Holland Publ. Co., Amsterdam 105-118
116. 1 complex. J. Biol. Chem. 274 (1999) 31209-31216
117. 1 with a photoreleasable decylubiquinol. Biochim. Biophys. Acta 1456 (2000) 121-137
118. Dutton P.L., and Prince R.C. Reaction center driven cytochrome interactions in electron and proton translocation and energy conservation. In: Clayton R.K., and Sistrom W.R. (Eds). The Photosynthetic Bacteria (1978), Academic Press, New York 525-570
119. 2 oxidoreductase from Rhodopseudomonas sphaeroides. Biochim. Biophys. Acta 635 (1981) 149-166
120. Bowyer J.R., and Crofts A.R. On the mechanism of photosynthetic electron transfer in Rhodopseudomonas capsulata and Rhodopseudomonas sphaeroides. Biochim. Biophys. Acta 636 (1981) 218-233
121. 1 complex of Rhodobacter capsulatus. In: Mathis P. (Ed). Photosynthesis: From Light to Biosphere: Proceedings of the Xth International Photosynthesis Congress vol. II (1995), Kluwer Academic Publishers, Dordrecht 547-550
122. Valkova-Valchanova M., Darrouzet E., Moomaw C.R., Slaughter C.A., and Daldal F. Proteolytic cleavage of the Fe-S subunit hinge region of Rhodobacter capsulatus bc(1) complex: effects of inhibitors and mutations. Biochemistry 39 (2000) 15484-15492
123. Cooley J.W., Ohnishi T., and Daldal F. Binding dynamics at the quinone reduction (Qi) site influence the equilibrium interactions of the iron sulfur protein and hydroquinone oxidation (Qo) site of the cytochrome bc1 complex. Biochemistry 44 (2005) 10520-10532
124. Paddock M.L., Feher G., and Okamura M.Y. Proton transfer pathways and mechanism in bacterial reaction centers. FEBS Lett. 555 (2003) 45-50
125. Wraight C.A. Proton and electron transfer in the acceptor quinone complex of photosynthetic reaction centers from Rhodobacter sphaeroides. Front. Biosci. 9 (2004) 309-337
126. Mulkidjanian A.Y., Cherepanov D.A., and Kozlova M.A. Ubiquinone reduction in the photosynthetic reaction center of Rhodobacter sphaeroides: interplay between electron transfer, proton binding and the flips of quinone ring. Biochem. Soc. Trans. 33 (2005) 845-850
127. Cherepanov D.A., Bibikov S.I., Bibikova M.V., Bloch D.A., Drachev L.A., Gopta O.A., Oesterhelt D., Semenov A.Y., and Mulkidjanian A.Y. Reduction and protonation of the secondary quinone acceptor of Rhodobacter sphaeroides photosynthetic reaction center: kinetic model based on a comparison of wild-type chromatophores with mutants carrying Arg→Ile substitution at sites 207 and 217 in the L-subunit. Biochim. Biophys. Acta 1459 (2000) 10-34
128. 2 in native and Glu-L212→Gln mutant reaction centers from Rhodobacter sphaeroides. Biochemistry 33 (1994) 1181-1193
129. Prince R.C., and Dutton P.L. Protonation and the reducing potential of the primary electron acceptor. In: Clayton R.K., and Sistrom W.R. (Eds). The Photosynthetic Bacteria (1978), Academic Press, New York 439-453
130. Shinkarev V.P., Mulkidjanian A.Y., Verkhovsky M.I., and Kaurov B.S. Investigation of the kinetic and thermodynamic properties of the photosynthetic reaction center secondary acceptor in chromatophore membrane of nonsulphur purple bacteria. Biol. Membr. 2 (1985) 725-737
131. Sled' V.D., Mulkidjanian A.Y., Shinkarev V.P., Verkhovsky M.I., Kaurov B.S., and Rubin A.B. Direct spectrophotometric determination of the midpoint potential of primary and secondary quinone acceptors of photosynthetic reaction center. Biokhimiya 49 (1984) 204-208
132. Crofts A.R., and Wraight C.A. The electrochemical domain of photosynthesis. Biochim. Biophys. Acta 726 (1983) 149-185
133. Zaslavsky D., Sadoski R.C., Rajagukguk S., Geren L., Millett F., Durham B., and Gennis R.B. Direct measurement of proton release by cytochrome c oxidase in solution during the F→O transition. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 10544-10547
134. Salomonsson L., Faxen K., Ädelroth P., and Brzezinski P. The timing of proton migration in membrane-reconstituted cytochrome c oxidase. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 17624-17629
135. Olsson M.H., Sharma P.K., and Warshel A. Simulating redox coupled proton transfer in cytochrome c oxidase: looking for the proton bottleneck. FEBS Lett. 579 (2005) 2026-2034
136. Raspe R.E. Singular Travels, Campaigns, and Adventures of Baron Munchausen (1948), Dover, New York
137. Jencks W.P. Catalysis in Chemistry and Enzymology (1987), Dover Publications Inc., New York
138. Mulkidjanian A.Y. Conformationally controlled pK-switching in membrane proteins: one more mechanism specific to the enzyme catalysis?. FEBS Lett. 463 (1999) 199-204
139. Humphrey W., Dalke A., and Schulten K. VMD: visual molecular dynamics. J. Mol. Graphics 14 (1996) 33-38
140. 1 complex. Biophys. J. 77 (1999) 1753-1768
141. 1 complex. Biochemistry 42 (2003) 1499-1507
142. 1 complex with its bound substrate cytochrome c. Proc. Acad. Sci. U. S. A. 99 (2002) 2800-2805