Ion Translocation Across Biological Membranes. Janos K. Lanyi University of California, Irvine
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1 Ion Translocation Across Biological Membranes Janos K. Lanyi University of California, Irvine
2 Examples of transmembrane ion pumps Protein Cofactor, substrate, etc. MW Subunits Mitoch. cytochrome oxidase hemes, Cu, Fe 130, Mitoch. cytochrome bc1 hemes, FeS, ubiquinone 225, Mitoch. ATPase ATP/ADP 350,000 >20 Mamm. NaK pump ATP/ADP 280,000 8 Mamm. Ca pump ATP/ADP 290,000 2 Bacteriorhodopsin retinal 24,000 1
3 Retinal based ion pumps (e.g. bacteriorhodopsin) 1. Energy input is photoisomerization of all-trans retinal to 13-cis,15-anti 2. Ensuing reaction cycle goes through intermediates K, L, M1, M2, M2, N1, N2, O, and back to BR 3. A proton is released to one side in the M2 to M2 reaction, and another is taken up from the other side in the N1 to N2 reaction 4. Net result of a turn-over (~ 10 ms) is transport of a proton
4 BACTERIORHODOPSIN a light-driven proton pump How does it work?
5 BACTERIORHODOPSIN a light-driven proton pump How does it work? More specifically: how does reisomerization of the 13-cis retinal drive steps 1-5?
6 BACTERIORHODOPSIN a light-driven proton pump A fundamental problem in ion pumps is: how local changes propagate to other regions of the protein to produce functionally relevant conformational changes
7 Images from Baudry, Tajkhorshid, Molnar, Phillips, Schulten, J.Phys.Chem. 105, (2001)
8 Frame 1, taken Aug 18-20, 2001 at beamline (ALS)
9 Frame 150, taken Aug 18-20, 2001 at beamline (ALS)
10 The BR state A chain of covalent and hydrogen-bonds links region of retinal to Asp-96 Hydrogen-bonded water at active center A hydrogen-bonded network links Asp-85 to Glu-194/Glu-204
11 5 retinal isomerizes retinal reisomerizes 4 retinal relaxes 1 3 switch 2
12 Species THE BR STRUCTURES Occupancy % Resolution Å PDB BR (wt) M0L K (wt), 100K M0K L (wt), 170K ~ O0A M1 (wt), 210K M0M M1 (wt), 295K P8H M2 (E204Q), 295K > F4Z M2 (D96N), 295K C8S N2 (V49A), 295K P8U
13 The Active Site (retinal Schiff base, a water, and the counter-ion/proton acceptor)
14 Schiff base Retinal geometry in non-illuminated and illuminated crystals (No restraints on angles used in refinement; starting models both all-trans and undistorted 13-cis) Models shown for L from three independent crystals, overlapped: note magnitude of crystalto-crystal variations in atomic positions
15 State C 13 angle Torsion angles* Torsion angles C 13 =C 14 C 14 -C 15 C 15 =NZ BR (n=2) 112, , , , -172 K (n=4) L (n=6) M 1 (n=3) M M Bond angle increases in K and gradually recovers during the first half of the photocycle
16 State C 13 angle Torsion angles Torsion angles C 13 =C 14 C 14 -C 15 C 15 =NZ BR (n=2) 112, , , , -172 K (n=4) L (n=6) M 1 (n=3) M M Deviations from ideal 13-cis,15-anti (torsion angles of 0 o, 180 o, and 180 o ) decrease between K and M2
17 - + all-trans retinal (BR) all-trans retinal - + idealized, relaxed 13-cis expected retinal 13-cis retinal cis retinal in K with strain, note increased C 13 bond angle
18 Retinal dynamics Step-by-step
19 BR Lys-216 retinal wat402 (Luecke et al, 1999; Schobert et al, 2002)
20 K photoisomerization (Schobert et al, 2002)
21 L relaxation (Lanyi & Schobert, 2003)
22 M 1 deprotonation (Lanyi & Schobert, 2002)
23 M 2 switch to other side (Luecke et al, 2000)
24 M 2 further relaxation (Luecke et al, 1999)
25 Conformational Cascades in the Protein (to conduct a proton to the extracellular surface and deliver a proton from the cytoplasmic surface )
26 The hydrogen-bonded network collapses and the positively charged arg-82 side-chain moves 1.7 Å down toward glu-194/glu-204 (color code: negative or positive charge)
27 The hydrogen-bonded network collapses and the positively charged arg-82 side-chain moves 1.7 Å down toward glu-194/glu-204 (color code: negative or positive charge) H +
28 Formation of a water cluster at Asp-96 2
29 BR M2
30 In N2 omit maps detect new density peaks modeled as water BR state BR plus N2
31 In N2 a hydrogen-bonded chain of four water molecules accumulates between the Schiff base and Asp-96 BR N2
32 In N there is a single-file hydrogen-bonded chain of four water molecules between the Schiff base and asp-96 H + BR N2
33 Tilt of helix F N-like state Subramaniam & Henderson, Nature 406, (2000) Tilt of helices A, B, C, D, and E O-like state Rouhani et al. J. Mol. Biol. 313, (2001)
34 CONCLUSION The principle of this ion pump is that the strain in the distorted photoisomerized retinal gradually relaxes as the binding site accomodates its changed shape. Inherently, the relaxation includes deprotonation of the Schiff base. The cascade of conformational changes that ensues allow release of a proton at one surface and uptake at the other.
35 Hypothesis: half-channels to the two membrane surfaces exist only to optimize transport 1. Mutations decrease turn-over but do not inactivate pump 2. Replacing the Schiff base counter-ion (Asp-85) with a Thr or Ser converts proton pump into a chloride pump 3. In eubacterial rhodopsins the extracellular proton release network is missing, but transport is not affected
36 1. Mutations decrease turn-over but do not inactivate pump Examples: Cytoplasmic side: D96N (absence of internal proton donor) prolongs lifetime of the deprotonated Schiff base Extracellular side: R82Q, E194Q, E204Q (absence of proton release group) delays proton release to the end of the cycle. Sequence of proton release and uptake is reversed.
37 2. Replacing the Schiff base counter-ion (Asp-85) with a Thr or Ser converts proton pump into a chloride pump Rationale: in halorhodopsin (a chloride pump) this residue is a Thr Clwt BR D85T BR HR Asp Asp Ala NH + Asp NH + Thr NH + Thr H + Cl -
38 3. In eubacterial rhodopsins the extracellular proton release network is missing, but transport is not affected Xanthorhodopsin (from Natronobacter ruber):
39 Differences between xanthorhodopsin and bacteriorhodopsin Particularly evident at the B-C and F-G interhelical loops
40 Cleft at the extracellular surface
41 Absence of extracellular network causes reversed release/uptake sequence
42 CONCLUSIONS The principle of this ion pump is that the strain in the distorted photoisomerized retinal gradually relaxes as the binding site accomodates its changed shape. Inherently, the relaxation includes deprotonation of the Schiff base. The cascade of conformational changes that ensues allow release of a proton at one surface and uptake at the other. The pump" resides in the active site. The two half-channels that connect it to the membrane surfaces do not play essential roles. They optimize turn-over.
43 Publications J Sasaki, LS Brown, Y-S Chon, H Kandori, A Maeda, R Needleman & JK Lanyi. Science 269, (1995). H Luecke, H-T Richter & JK Lanyi, Science, 280, (1998). H Luecke, B Schobert, H-T Richter, J-P Cartailler & JK Lanyi, J. Mol. Biol. 291, (1999). H Luecke, B Schobert, H-T Richter, J-P Cartailler & JK Lanyi, Science 286, (1999). H Luecke, B Schobert, H-T Richter, J-P Cartailler, A Rosengarth, R Needleman & JK Lanyi, J. Mol. Biol. 300, (2000). B Schobert, J Cupp-Vickery, V Hornak, SO Smith & JK Lanyi, J. Mol. Biol. 321, (2002). JK Lanyi & B Schobert, J. Mol. Biol. 321, (2002). JK Lanyi & B Schobert, J. Mol. Biol. 328, (2003). B Schobert, LS Brown & JK Lanyi, J. Mol. Biol. 330, (2003). SP Balashov, ES Imasheva, VA Boichenko, J Antón, JM Wang & JK Lanyi, Science 309, (2005). JK Lanyi & B Schobert, J. Mol. Biol. 365, (2007). H Luecke, B Schobert, J Stagno, ES Imasheva, JM Wang, SP Balashov & JK Lanyi, Proc. Natl. Acad. Sci. U. S. A. 105, (2008).
44 Thanks to: H.T. Richter B. Schobert L. Brown A. Dioumaev D. Chen S.P. Balashov E. S. Imasheva JM Wang Collaborators R. Needleman, Wayne State A. Maeda, Kyoto Univ. H. Luecke, Univ. Cal. Irvine J. Cupp-Vickery, Univ. Cal. Irvine S.O. Smith, Stony Brook (and their co-workers) Funded by grants from NIH, DOE, and US Army Research Office Beamlines at ALS, SSRL, SPring-8 and ESRF
45
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